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Home , Neuroethology, Sensory maps, Sound localization

Neuroethology in or Why study an exotic animal Nobel prize in Physiology and Medicine 1973

Karl von Frisch for their discoveries concerning "organization and elicitation of individual and social behaviour patterns".

Behaviour patterns become explicable when interpreted as the result of , analogous with anatomical and physiological characteristics. This year's prize winners hold a unique position in this field. They are the most eminent founders of a new science, called "the comparative study of behaviour" or "" (from ethos = habit, manner). Their first discoveries were made on insects, fishes and birds, but the basal principles have proved to be applicable also on mammals, including man. Nobel prize in Physiology and Medicine 1973

Karl von Frisch Konrad Lorenz Nikolaas Tinbergen Ammophila the sand wasp

Black headed gull Niko Tinbergen’s four questions? 1. How the behavior of the animal affects its survival and reproduction (function)? 2. By how the behavior is similar or different from behaviors in other species (phylogeny)? 3. How the behavior is shaped by the animal’s own experiences (ontogeny)? 4. How the behavior is manifested at the physiological level (mechanism)? as a sub-field in research • A large variety of research models and a tendency to focus on esoteric animals and systems (specialized behaviors). • Studying animals while ignoring the relevancy to humans. • Studying the brain in the context of the animal’s natural behavior. • Top-down approach.

Archer fish

Prof. Ronen Segev Ben-Gurion University Neuroethology as a sub-field in brain research • A large variety of research models and a tendency to focus on esoteric animals and systems (specialized behaviors). • Studying animals while ignoring the relevancy to humans. • Studying the brain in the context of the animal’s natural behavior. • Top-down approach.

דג חשמל נמוכי מתח Weakly Jamming avoidance response Neuroethology as a sub-field in brain research • A large variety of research models and a tendency to focus on esoteric animals and systems (specialized behaviors). • Studying animals while ignoring the relevancy to humans. • Studying the brain in the context of the animal’s natural behavior. • Top-down approach.

Place Cells

1.5 m Neuroethology as a sub-field in brain research • A large variety of research models and a tendency to focus on esoteric animals and systems (specialized behaviors). • Studying animals while ignoring the relevancy to humans. • Studying the brain in the context of the animal’s natural behavior. • Top-down approach.

Some classical models in neuroethology Neuroethology where to?

• The field is moving away from the neuroethological approach by focusing on rodent models and neglecting all other species. • The field is moving towards neuroethology by studying directly the physiology of behavior and by addressing natural behaviors that are relevant to the mouse.

• localization

• plasticity and development

•Spatial attention

•Multisensory integration Barn as model system for • Facial ruff serves as a sound amplifier Barn owls as model system for sound localization • Facial ruff serves as a sound amplifier • Asymmetric allow for an increased spatial resolution in the vertical plane Barn owls as model system for sound localization • Facial ruff serves as a sound amplifier • Asymmetric ears allow for an increased spatial resolution in the vertical plane • Comb-like structures at the leading edge of the wing reduce noise during flight Barn owls as model system for sound localization Facial ruff serves as a • sound amplifier Asymmetric ears allow for • an increased spatial resolution in the vertical plane Comb-like structures at the • leading edge of the wing reduce noise during flight Brain structures involved • in the analysis of sound are enlarged Performing a psychoacoustic experiment with an Sound-localization with free-field stimuli • The auditory localization cues:

• ITD - horizontal ILD - vertical

location producing ITD = 0 µsec

location producing ITD = 100 µsec

Precision of sound localization in barn owls may be as good as 3 deg which corresponds to 6-10 µs. Action Postsynaptic potential potentials

These signals are the “language" of neural processing. Durations of events

• Typical duration of action potential: 1ms • Typical duration of post-synaptic potentials: 5-10 ms • Precision of sound localization by interaural time difference: 6-10 µs

What has to be explained is

Factor of 500-1000

The principle of phase locking as a means to conserve time Sinusoidal signal

Presumed resulting post- synaptic potential

Registered signal in computer

Note that in this example the response always occurs at a phase of 180 degrees. Phase locking in the barn owl

Phase locking can be measured by plotting spike arrival times with respect to the period of the tone.

5 kHz Period 200 µs 9 kHz Period 111 µs spikes number of

Stimulus phase in degrees

Precision of phase locking is 35 µs at 5 kHz (Koeppl (1997)). Jefferess model (1948)

Ai + Ni = Ac + Nc

Ai − Ac = Ni − Nc

ITD

left Right ear Delay lines Does the brain computes ITDs as Jefferess suggested?

Nucleus Laminaris / Medial Superior Olive - sites of binaural convergence Anatomical evidence for Jeffress model ITD curves in Nucleus Laminaris s) µ ITD(

Response

Time (ms) ITD (µs) SOUND LOCALIZATION GAZE CONTROL

Forebrain Sensory/Association Archistriatum Areas (FEF)

Thalamus Ovoidalis Rotundus (MGN) (Pulvinar)

Inferior Inferior Optic Tectum Midbrain Colliculus Colliculus central n. external n. (SC) D R

VLVp (LSO/DNLL) Brainstem Tegmentum LAM (MSO)

Motor Nuclei left right for gaze control cochlear n. cochlear n. Response +20 20 ILD (dB) ILD 0

0 el V - 20 -20

R20 L20 0 az Response

-50 0 50 ITD (µs) +20 20 V (dB) ILD

0 el 0

- 20 -20

R20 L20 0 az Response

-50 0 50 ITD (µs) Visual and auditory maps in the OT Computational map

Transducing Computing Integrating cues Associating with sound to auditory localization from specific external space action-potentials cues locations

Sound Frequency Space tuned Frequency Intensity Binaural localization cues Time Side of ear Computational maps The matching problem

location producing ITD = 0 µsec

location producing ITD = 100 µsec Computational maps The matching problem

location producing ITD = 0 µsec

location producing ITD = 100 µsec

Normal Immediate Effect Prism-adapted of Prisms Knudsen and Knudsen J Neurosci (1989) Effect of prism experience on auditory tuning

Normal Immediate effect of prisms

+20 A A V V 0 el -20

L20 R20 0 az

Knudsen and Brainard, Science (1991) Effect of prism experience on auditory tuning

Normal Immediate effect After 8 weeks of of prisms prism experience

+20 A A A V V V 0 el -20

L20 R20 0 az Quantification of

1. Behavioral test 2. Physiological test Decline in learning with age

6 7 Knudsen, E. I. .Science.(1998) . Increased capacity for learning in adults that have had appropriate experience as juveniles

6 7 Knudsen, E. I. .Science.(1998) . Effects of juvenile experience on adult learning

6 7 Knudsen, E. I. .Science.(1998) . Incremental learning

170 110 60

230 Incremental learning

Linkenhoker and Knudsen (2002) Nature Rich and lively experiences increase learning capacity in adults

Bergan et al., Journal of Neuroscience (2005) Summary

• Decline in learning with age • Increased capacity for learning in adults that have had appropriate experience as juveniles • Incremental training improves learning • Rich and lively experiences increase learning capacity in adults Where is the site of plasticity?

Forebrain Sensory/Association Archistriatum Areas (FEF)

Thalamus Ovoidalis Rotundus (MGN) (Pulvinar)

Inferior Inferior Optic Tectum Midbrain Colliculus Colliculus central n. external n. (SC)

VLVp (LSO/DNLL) Brainstem Tegmentum LAM (MSO)

Motor Nuclei left right for gaze control cochlear n. cochlear n. Horizontal section through the tectal lobe

Visual input from Retina and Forebrain

c 00

r

00

0 200 20 ICC

400

ICX 400

OT r m l c Site of plasticity in the ICX

Debello et al., J. Neurosci. 2001 After prism learning

Visual input from Retina and Forebrain

c 200

r

200

0 400 40 ICC

600

ICX 600

OT r m l c The instructive signal

- Operates in the ICX

- Visually based

Where is the instructive signal coming from? BDA injection site in ICX

250 µm Topography of the OT-ICX projection

Layer 8

BDA

FG

r l Restricted lesion of the optic tectum

r l 500 µm How can a visually based instructive signal act in an auditory structure? Horizontal section through the tectal lobe

Visual input from Retina and Forebrain

c 00

r

00

0 200 20 ICC

400

ICX 400

OT r m l c bicuculline

recording

bic 0 iontophoresis barrels recording barrel rec 0

50 50 ICC 100 100 µsec 500 µm ICX OT

r m l c Light responses in the ICX Visual Receptive Fields in the ICX ICX OT ICX OT 0 µm

bic

-150 µm

ICX

-300 µm

OT -450 µm

-600 µm

Properties of visual responses in ICX

- Arrive from the OT

- Display spatially restricted visual receptive fields

- Form a map of space

- Align with auditory spatial representation Model gate

ITD 1 Visual Input

Visual Input ITD 2

ITD 3 ITD 1 Visual Input

Visual Input ITD 2

ITD 3

Input Auditory ITD 1 Visual Input

Visual Input ITD 2

ITD 3 ICX Optic Tectum Bimodal Stimulus

light right ear left ear Visual and auditory interactions in ICX in the Visualinteractions auditory and

ITD auditory auditory

visual visual +

Average

60 12 14

30 8 s) µ 10 A (spikes) A

0 - ITD ( AV

6 4 A (spikes) A -30 - AV

6 0 -60

50 100 150 200 -80 -60 -40 -20 0 20 40 60 80 Post stimulus time (ms) ITD (µs) Bimodal stimulus

Normal

Visual input

ICC

ICX

OT Bimodal stimulus

Normal With prisms

Visual input Visual input

ICC ICC

ICX ICX

OT OT Bimodal stimulus

Normal With prisms

Visual input Visual input

ICC ICC

ICX ICX

OT OT Summary

An inhibitory gate controls the flow of visual • information into the

Summary

• An inhibitory gate controls the flow of visual information into the auditory system

• The visual signals are appropriate to serve as the instructive signal for auditory plasticity

• Eric Knudsen Daniel Feldman Michael Brainard Will Debello Stanford University Peter Hyde Brie Linkenhoker Joe Bergan

Hermann Wagner - AACHEN University