Learningin Birds--

And how it relates to learning in us.

Timothy DeVoogdCornell University

(Attempting tocatch birds for

research)

My own initial rationale was simple curiosity about brain function and brain plasticity (and I had become allergic to rats in grad school).

I assumed some sort of similarity to humans, without thinking much about why this would be or how it would have arisen.

Why Study Birds?

Because what we learn can show us what our brains might do: birds as “a model system” for human biology.

But what do you tell NIH or Colciencias (“Health Relevance”),

or your cousins (“Tim, are you still studying bird brains” [muted laughter])

Model System

• If we’re honest, this seems unlikely:– Birds are not closely

related to us– Their brains are very

different• (nothing that looks like

cortex• No corpus callosum• Different layout (and

names!) of other regions

– Their activities also seem too different

Bird Song Learning“How does a bird’s brain learn song?

Spatial Learning“How do birds rememberplaces?”

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Baby Songbirds are Altricial at Hatching

Songs of Normally Reared Sparrows

Songs of Sparrows Reared in Isolation

1. In most songbirds, males do all or most of the singing. Females sing little or not at all.2. Young males learn their songs from adult males3. As adults, males of many species attract females with song4. Singing occurs with reproduction For many species outside of the tropics, this is seasonal5. Different species vary in how complex a song they typically sing

6. For all species but those with the simplest song types, males within a species also differ in song complexity

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Song Facts

Causation• Determine the physical structures

that produce song– Syrinx, at the opening of two bronchi– Beak and tongue movements

• Map how the brain controls these– Songbird song is produced using the

motor song system, a group of brain regions that are highly interconnected.

• Map correlations between brain structure and function– Across sexes and seasons– Between and within species

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The Motor Song System consists ofProduction (red) and Regulatory Nuclei (blue)

[No obvious correspondence to mammal forebrain in general layout or in specific structures]

Red paths: for productionBlue: originally unknown,

Relations to Learning

• HVC and RA are essential for song production. Could they be involved in the learning? Our approaches:– A. Comparative study across species– B. Study of variation within species– C. Experimental manipulation of opportunity to

learn

DeVoogd, Székely & Büki--part of the Hungarian work crew

HVC / RA Predicts Learning Ability

Comparisons across more closely related clades

(groups of species) yields better comparability

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Syllable Repertoire can Vary by Nearly Two Orders of Magnitude

Between Warbler Species

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HVC HVC

Marsh Warbler River Warbler

Differences in HVC Volume Between Species can be Striking--And they parallel song complexity

Székely et al., ‘96

Airey & DeVoogd, ‘00

-2

0

2

-0.075 0.000 0.075

Relative HVC Volume

RelativeRepertoire

Sizer = 0.52, p < .02

B. Variation Within a Species:HVC Volume and Repertoire

Size are Positively Correlated in Zebra Finches

Volumes of brain areas may be poor measures of processing capacity--the

actual job of the brain.

This may be more closely estimated by assessing cell number, and integrating this with axonal, dendritic and synaptic

distribution (i.e. connection information)

Song System: Golgi Stained RA Neurons

RA

[Not like cortical neurons]

C. Manipulate Opportunity to Learn: Male Zebra Finches Reared in Isolation

Have Abnormally Simple Song andFewer Spine Synapses in HVC

Lauay, Komorowski & DeVoogd, 2005

0

5

10

15

20

25

30

Social Deprived Isolate

Number ofSpines / 12µm

of Dendrite

p < .05

Song is interactive:Accurate decoding is as important

as accurate production.Thus, if a male is encoding complexity

and is singing to a female, the female must be able to assess

the complexity.

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Females Monitor Male Songand Use it in Selecting Mates

Bensch & Hasselquist, ‘92

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Hearing Song Activates Novel Brain Regions

7

8

9

NS

0

1

2

3

4

5

6

Social Rearingn = 9

p < 0.05

Deprived Rearingn = 9

Isolate Rearingn = 8

NSNumber of

Females

Female Zebra Finches LearnSong Discrimination

Lauay et al., 2004

SocialIsolate

Female Finches Reared in IsolationHave Fewer Spine Synapses in NCM

Lauay, Komorowski & DeVoogd, 2005

Mean Number ofSpines / 12µm of

Dendrite

*

0

5

10

15

20

25

30

35

40

45

50

Males Females n=5 n=7 n=6 n=5

Control

Song Deprived

Summary

• A dedicated “song system” is used to produce song

• These areas are also responsible for song learning– Variation in size gives different capacities, – Opportunity to learn song causes plastic

changes in synapses

Creates thousands of scattered food caches in FallUses memory to retrieve caches during winter

An Adaptation in Spatial Memory- Food-storing Birds

Anatomy of the Avian Hippocampus

•Location: Surface of the Brain•Inputs from the Septum and Cortex-like Areas

BUT…•No 3-layer organization•No tri-synaptic pathway•No DG or other mammal- like components

Hippocampal Lesions Impair Spatial Memory

[Sherry & Vaccarino, 1989]0

20

40

60

80

% v

isits

Hp HA Control

Sherry & Vaccarino, ‘89

Caching was unimpaired

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Inactivating Hp at Acquisition-- Prevents Spatial Memory Acquisition,

No Deficit in Cue-based Memory

•Infuse with 2% lidocaine prior to memory acquisition

•Assess memory acquisition across 5 trials

Shiflett et al (2003) Hippocampus

Inactivating Hp at Retrieval--Disrupts Recent Memory

No Deficit for Remote Memory

Shiflett et al (2003) Hippocampus

In mammals, NMDA receptors:1) Are coincidence detectors

2) Activate second messenger systems within neurons

3) That can change synaptic strength directly

4) Or by activating Immediate Early Genes

5) That then turn on Late Effector and Regulatory Genes

6) To create structural and regulatory proteins

1

2

3

4

5

6

NMDA-R InactivationImpairs Acquisition,

Does not Impair Retrieval

Infuse with AP5 prior to memory acquisition or memory retrieval

Shiflett et al (2004) Behav. Neurosci

In mammals, the hippocampus has high levels of receptors for steroids from adrenal cortex

Chronic stress (which causes the steroids to be released) or steroid administration causes hippocampal shrinkage (for ex., humans--PTSD, rats--chronic restraint)

10

12

14

16

18

20

Hp

Vol

ume

225 250 275 300 325 350

Tel Volume

Lab

Wild

Captivity Causes the BCC Hp to Shrink

12 birds capturedin Dec.

Half released,half lab-housed

After 5 weeks, wild ones wererecaptured. Tel and Hp measured in all.

Tarr et al., in press

Hippocampus Conclusions

• The hippocampus is used to encode spatial memory in birds as it is in mammals

• Molecules like NMDA receptors must be activated to form LTM, as in mammals

• The hippocampus pays for its ability to learn rapidly by being sensitive to stress, as in us

1. Different forms of learning in birds use different brain systems

2. Song learning is slow and enduring, and requires links from motor areas to muscles

3. Spatial learning is rapid but fragile and requires the hippocampus to form it, but not to preserve it

Summary

So what? Do birds teach us

anything about

ourselves?

• Motor cortex sends movement signals to spinal cord

• Motor activity is modulated by the basal ganglia

• Motor cortex cells project to basal ganglia, which then project to thalamus, and back to the cortex

Motor Cortex

The Motor Song System consists ofProduction (red) and Regulatory Nuclei (blue)

The Motor Song System consists ofProduction (red) and Regulatory Nuclei (blue)

(Or areas like human pre-motor and motor cortex and basal ganglia)

In addition, an area homologous to amygdala is used for emotional learning

Altering Influences on Song SystemNuclei in Adults can Alter their Output

NormalCanary

Kitko & DeVoogd, in prep.

lMANlesion

Different Forms of Learning in Humans use Different Brain Regions

Fast, factual, Slow, precise,modifiable[Hp] resists change

Different Forms of Learning in Humans use Different Brain Regions

Different Forms of Learning in Humans use Different Brain Regions

• Reading words in a mirror (as in class)

• Patients are just like controls if new sets of words are given (left), but less good than controls if words are used again (right). [Why?]

The Brain of Vertebrates

Nieuwenhuys et al., (1998)

Last commonancestors

were reptile-like

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Kumar & Hedges, 1998

: Brain Systems:

Learning is divided into similar behavioral classes in birds and mammals.

They use brain systems that are alike both in networks and mechanisms to deal

with these classes.

This must be because these functional distinctions evolved in remote ancestors

and have been preserved ever since

Molecular Implications:

1)The molecular basis of synaptic plasticity evolved very earlyand has been highly conserved.

4)Understanding how each molecule hands off function to the next is a powerful means of addressing disease.

Functional Implications:

If you want to understand normal function:Learn about essential features of the behaviorLearn about the brain modifications that give a particular species its abilities

Thus, if you want to know how our cognition differs from a mouse, and how various forms of memory are organized across the brain, consider studying unusual systems, even birds!

And Finally Back to my Cousins…

• Yes, I’m still studying bird brains• I’ve observed that birds are amazingly bright• I’ve discovered a bit about how their brains do

it• Because the brains are so different, the birds are

helping to show me essential ways about how our brains work

¡Muchas Gracias!

What about brain systemsinvolved in learning?

Humans also use different brain systems for different forms of learning

System Implications:

1) Molecular description is unlikely to explain our memory of time or of faces, etc.

2) Using model systems that seem esoteric could be a powerful means of describing “essences”--the features that are necessary for a particular function.

3) Thus, know your question--do you want to describe and possibly fix a malfunction? Study molecules.

4) Or do you want to understand normal function--how our cognition differs from a mouse, and how various forms of memory are organized across the brain? [And if the latter, consider unusual systems!]

Molecular:

The units (synapses, molecules) for building memory, and the sequence in which they are used are the same.

7) Species differences in these systems matches behavioral capacity

8) Natural learning can easily be studied in birds

9) Birds are great for comparative and evolutionary questions