vestibular signals jan van gisbergen

VESTIBULAR SIGNALS

Jan Van Gisbergen

PhD COURSE SENSORY SYSTEMSUtrecht, September 29, 2008

detection of self motion sensing body orientation in space visual perception in earth-centric coordinates

SCOPE

Functions and limitations of vestibular sensors

Ambiguity problem of the otoliths

Solution to the ambiguity problem

Visual-vestibular fusion

Transformations from head to body reference frame

Visual space perception in static tilt

Bayesian model

MULTISENSORY INTEGRATION

VESTIBULAR SENSORS

functions &

limitations

VESTIBULAR SENSORS

canals

otoliths

SEMICIRCULAR CANALS

measure head rotation

CANAL GEOMETRY

Three perpendicular canals measure head rotation in 3 dimensions

BEST ROTATION AXES

a = anterior canal

p = posterior canal

h = horizontal canal

rotation in direction of arrow excites afferents from a given canal

BEST ROTATION AXIS OF CANAL AFFERENT

Yakushin (2006) JNP

OPTIMAL ROTATION AXES OF CANAL AFFERENTS

DYNAMICS OF CANAL SIGNALS

Insensitive to low-frequency rotations (high pass filter)

Canal afferent fiber in 8th nerve• High resting discharge• Codes cupula deviation

CONSTANT ROTATION IN DARKNESS

• rotation percept decays

• after stop, percept of rotation in opposite direction

• reflects cupular mechanics

OTOLITHS

sensitive to linear acceleration during translation and to tilt, due to the pull of gravity

HAIRCELL ACTIVATION

• each haircell is connected to separate nerve fiber

• deflecting cilia toward kinocilium depolarizes haircell

POLARISATION VECTOR

Eron et al. (2008) J. Neurophysiol.

each otolith cell has cosine tuning:

indicates head orientation where pull of gravity has maximum effect

tilt stimuli:

nose down left ear down nose up

OTOLITHS

sensitive to tilt and translation

POLARISATION VECTORS

Fernandez and Goldberg (1976) JNP

AMBIGUITY PROBLEMOF THE OTOLITHS

OTOLITH SIGNAL IS AMBIGUOUS

hair cells cannot distinguish tilt and translation

SOMATOGRAVIC ILLUSION

pilot is upright, but feels tilted

(only in darkness)

AMBIGUITY PROBLEM

otolith signal may have various causes:

• translation (a)• force of gravity due to tilt (g)• combination of a and g

How can the brain resolve this ambiguity ?

inverse problem

CANAL- OTOLITH INTERACTION MODEL

• canals detect rotation during tilt changes

• their signal helps to decompose otolith signal

Angelaki et al. (1999)

CANAL–OTOLITH INTERACTION MODEL

basic principle:- tilt stimulates otoliths AND canals- translation stimulates only otoliths

Merfeld and Zupan (2002) J. Neurophysiology

tilt angle

linear acceleration

angular velocity

percepts during rotation about a tilted axis

(OVAR)

Vingerhoets et al. (2006) J. Neurophysiol.

Vingerhoets et al. (2007) J. Neurophysiol.

TESTING THE MODEL

THE ACTUAL MOTION

- rotation about tilted axis

- in darkness

- constant velocity

MODEL PREDICTIONS

rotation signal decays gradually

wrong interpretation otolith signal: illusory translation percept

SCHEMATIC SUMMARY OF RESULTS

confirms prediction

rotation percept

translation percept

Actual motion:

Percept:

TRANSLATION AND ROTATION PERCEPT DATA

rotation percept

translation percept

VISUAL – VESTIBULAR FUSION

FUSION OF VISUAL AND VESTIBULAR SIGNALS FOR DETECTION OF

EGOMOTION

• brain interprets whole field motion as due to egomotion

• can detect constant velocity motion (low pass)

• complements vestibular motion detection (high pass)

CANALS ARE HIGH PASS

ROTATION IN LIGHT: VISUAL CONTRIBUTION

• Rotation percept in the light is veridical

• Visual system detects low frequencies

• Canals detect high frequencies

circular vection

CONVERGENCE IN VESTIBULAR NUCLEUS

visual system detects low frequencies

canals detect high frequencies

OPTIC FLOW PROVIDES LOW FREQUENCY INPUT FROM LINEAR MOTION

• otoliths detect linear acceleration

• optic flow can induce linear egomotion (train illusion!!)

TRANSFORMATIONS FROM HEAD TO BODY

REFERENCE FRAME

BALANCE

1. Otoliths measure head position in space

2. To maintain balance, we must know body position in space

3. Which mechanisms are involved?

BALANCE

1. Measure head position in space (HS)

2. Measure position head on trunk (HB)

3. Compute position of body in space (BS):

BS = HS - HB

EFFECT OF ELECTRICAL OTOLITH STIMULATION

•experiment in darkness

•results in body tilt

Why?

HS changes

HB is not changed

BS changes, subject corrects

BS = HS - HB

VESTIBULAR - NECK PROPRIOCEPTIVE INTERACTIONS

neuron b codes linear motion in body-centered reference frame (accounts for neck signals)

neuron c codes motion in head-reference frame

Angelaki (2008) Ann Rev Neuroscience

monkey moves on sled in various directions

cell recording in cerebellum (FN)

VISUAL SPACE PERCEPTION IN

STATIC TILT

VISUAL VERTICAL

1. How can we determine the orientation of visual objects relative to the direction of gravity, even when we are tilted in darkness?

2. What is the role of the vestibular system?

SENSING THE DIRECTION OF GRAVITY

Two different tasks:

1. Set line to vertical (SVV)

2. Estimate your body tilt (SBT)

Van Beuzekom & Van Gisbergen (2000) J. Neurophysiol.

Van Beuzekom et al. (2001) Vision Res.

Kaptein & Van Gisbergen (2004, 2005) J. Neurophysiol.

De Vrijer et al. (2008) J. Neurophysiol.

experiments in darkness

ACCURACY vs PRECISION

Accuracy:

How close is the response to the true value?

Precision:

How reproducible is the response?

darts analogy:

ACCURACY AND PRECISION IN LINE TASK (SVV)

accuracy

precision

De Vrijer et al. (2008) J. Neurophysiol.

De Vrijer et al. (2008) in progress

ACCURACY IN LINE TASK

due to underestimation of body tilt?

NO UNDERESTIMATION OF BODY TILT

SVV SBT

• Subjects know quite well how they are tilted (SBT)

• Yet, their line settings undercompensate for tilt (SVV)

Van Beuzekom et al. (2001) Vision Res.

Kaptein and Van Gisbergen (2004) J. Neurophysiol.

PRECISION IN LINE TASK

is scatter in SVV simply reflection of noise in body tilt signal?

De Vrijer et al. (2008) J. Neurophysiol.

De Vrijer et al. (2008) in progress

SVV LESS NOISY THAN SBT

De Vrijer et al. in progress

psychometric experiments at 0o and 90o tilt:

SVV LESS NOISY THAN SBT

SUMMARY SBT AND SVV DATA

Two paradoxical findings:

1. subject knows tilt angle, yet makes biased line settings

2. more certain about line setting than about body tilt

estimate body tilt (SBT) adjust line to vertical (SVV)

SBT DATA SHOW:

• An unbiased head tilt signal is available

• Noise increases with tilt angle

SIGNALS REQUIRED FOR SPATIAL VISION

retinal signal

to compute line in space (Ls), brain must combine info about line orientation on retina (LR) and head tilt (HS)

head-tilt signal

SIMPLY USING RAW TILT SIGNAL …

would not explain SVV bias !!spatial vision would be accurate, but noisy

raw tilt signal

A BAYESIAN PERSPECTIVE

IDEAL OBSERVER MODEL

IDEAL OBSERVER STRATEGY

1) Use sensory data: noisy tilt signal suggests range of possible tilt angles (likelihood)

2) Use prior knowledge: we know that large tilt angles are very uncommon (prior)

3) Most likely tilt angle (posterior) is product of likelihood and prior

Eggert (1998) PhD Thesis, Munich

MacNeilage et al. (2007) Exp. Brain Res.

De Vrijer et al. (2008) J. Neurophysiol.

IDEAL OBSERVER STRATEGY

Tilt prior has 2 effects on SVV:

• Less noise

• Bias at large tilt

WHY WOULD THIS MAKE SENSE?

1) Less noise in spatial vision

2) Downside: bias at large tilts

3) Average performance improves (large tilts are rare)

DEMO

BIAS EFFECT INCREASES WITH TILT

no bias

De Vrijer et al. (2008) J. Neurophysiology

no bias

small bias

small bias

large bias

large bias

MODEL PARAMETERS

1) head tilt noise level in upright

2) increase of head tilt noise with tilt

3) prior width

4) eye torsion amplitude

MODEL FITS: SVV ACCURACY

MODEL FITS: SVV ACCURACY

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QUESTIONS1) The canal-related neuron illustrated in the paper by Yakushin (see slide 10 in lecture) can be

identified by its excitatory and inhibitory responses to sinusoidal rotation about various axis orientations relative to the head.

a)      What would happen if the same head-fixed rotations would be applied, but now with the animal in supine position, rather than in the prone position shown in the figure? Explain your answer.

b)      Sketch expected response patterns for a neuron getting its input from the right anterior canal, when using the same rotation axes as shown in the lecture sheet?

c)      Estimate the frequency of rotation and explain why its choice is important

2) In the scheme showing how combining a signal Hs and a signal coding Hb can yield a signal body orientation in space (Bs), the two input signals have opposite signs (see slide 38).

a)      Explain why this makes sense, given the fact that we can tilt the head and still remain upright

b)      Explain why electrical otolith stimulation does cause perturbation of balance

MODEL EXPLANATION OF NOISE LEVELS:SVV vs SBT PRECISION

• SVV is less noisy than the SBT (remarkable, but explained by model)

• SBT becomes more noisy at larger tilt (supports model assumption)

• SBT noise levels compatible with head-tilt fit results

CONCLUSION

Accuracy-precision trade-off in spatial vision:

• Bayesian strategy reduces noise at small tilts

• causes systematic errors at large tilts

CENTRIFUGE EXPERIMENT

proefpersoon wordt in donker langdurig rondgedraaid op centrifuge

• draait nog steeds rond maar voelt geen rotatie meer

• zit in feite rechtop maar voelt zich gekanteld

OVAR

TWO TRANSFORMATIONS OF PRIMARY VESTIBULAR SIGNALS

1. Signals from the canals (ω) are used to decompose signals from otolith afferents (α) into gravitational (g, orientation) and translational (f) components.

2. Gravitational estimates are also used to transform head-fixed angular velocity signals from the

semicircular canals (ω) into inertial velocity, i.e., space-referenced angular velocity (ωs)