What are we trying to explain multiple facets of a simple behavior
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What are we trying to explain? Multiple facets of a simple behavior. Stephen G. Lisberger Howard Hughes Medical Institute W.M. Keck Center for Integrative Neuroscience Department of Physiology, UCSF. What we are trying to explain. What does Barry have to do to hit a home run?.

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What are we trying to explain multiple facets of a simple behavior

What are we trying to explain?Multiple facets of a simple behavior

Stephen G. LisbergerHoward Hughes Medical Institute

W.M. Keck Center for Integrative NeuroscienceDepartment of Physiology, UCSF


What we are trying to explain

What we are trying to explain


What does barry have to do to hit a home run

What does Barry have to do to hit a home run?

  • Sense ball motion and determine speed and direction of motion.

  • Decide whether or not to swing the bat.

  • Program the correct swing to meet the ball just in front of his right foot.

  • Make any corrections as the ball “moves”.

  • All in 400 ms!


What we are trying to explain simplified

What we are trying to explain, simplified


Methods for studying pursuit eye movement

Methods for studying pursuit eye movement


The behavior pursuit eye movements

The behavior: pursuit eye movements


Smooth pursuit in the time domain

Smooth pursuit in the time domain


Target motion versus image motion

Target motion versus image motion


Anatomy of pursuit

Anatomy of pursuit

Why are there so many different parts to the pursuit circuit?

Perhaps each part of the circuit is doing a different computation.

Caudate

nucleus


What are we trying to explain multiple facets of a simple behavior

The signals recorded in different areas are more similar than different: consider motor cortex (FPA), parietal cortex, and the cerebellum during pursuit

  • Transient and sustained responses

  • Directional tuning

  • Firing related to target speed

  • Similar latencies


Neurons in the fpa fire nicely during pursuit

Neurons in the FPA fire nicely during pursuit


Neurons in the cerebellum also fire nicely during pursuit

Neurons in the cerebellum also fire nicely during pursuit


Even neurons in the parietal cortex in area mst fire nicely during pursuit

Even neurons in the parietal cortex -- in area MST -- fire nicely during pursuit


What are we trying to explain multiple facets of a simple behavior

Neural responses during the behavior don’t distinguish different parts of the pursuit circuit -- now what?

  • It’s especially troubling that all of these areas combine similar blends of signals related to eye velocity, head velocity, and visual motion.

  • The same would be true in the basal ganglia, probably.

  • The same would probably be true for neural activity related to Barry’s home run swing.

  • So, let’s look at the behavior and see if we can use similar signals to support different behavioral features.


What are we trying to explain the many features of the pursuit behavior

What are we trying to explain -- the many features of the pursuit behavior.

  • Smooth eye movement persists without image motion.

  • Population decoding for visual-motor transformations (probably done at multiple levels)

  • On-line gain control

  • Target choice in real-world situations

  • Long-term adaptive changes (learning)


What are we trying to explain the many features of the pursuit behavior1

What are we trying to explain -- the many features of the pursuit behavior.

  • Smooth eye movement persists without image motion.

  • Population decoding for visual-motor transformations (probably done at multiple levels)

  • On-line gain control

  • Target choice in real-world situations

  • Long-term adaptive changes (learning)


Natural inputs show that image motion goes away during accurate pursuit

Natural inputs show that image motion goes away during accurate pursuit.

Visual input consists of a big pulse of image motion

…followed by a time of very little image motion and big sustained eye motion


Continued tracking during image stabilization provides evidence for eye velocity memory

Continued tracking during image stabilization provides evidence for “eye velocity memory”


What are we trying to explain multiple facets of a simple behavior

A simple feedback controller won’t show velocity memory, and requires high internal gain to achieve excellent tracking

-

T

+

I

E

+

g

E = g I = g (T – E) = gT – gEE + gE = gTE (1 + g) = gTGain = E / T = g / (1+g)

Gain is 0.5, if g = 1Gain is 0.9, if g = 9

Gain is 0.99, if g = 99


An idea about how to create velocity memory with a positive feedback circuit

An idea about how to create velocity memory with a positive feedback circuit

Lisberger, Exp. Brain Res. Suppl 6: 501-514, 1982.

What discharge would we expect if we recorded from F? Signals related to eye velocity. MST, FPA, and the cerebellum all potentially qualify. But this is a nuts-and-bolts function and we imagine it is supported by cerebellar circuits.


What are we trying to explain the many features of the pursuit behavior2

What are we trying to explain -- the many features of the pursuit behavior.

  • Smooth eye movement persists without image motion.

  • Population decoding for visual-motor transformations (probably done at multiple levels)

  • On-line gain control

  • Target choice in real-world situations

  • Long-term adaptive changes (learning)


How do we think about visual motor transformations in terms of neural circuits

How do we think about visual-motor transformations in terms of neural circuits?

Parieto-ponto-cerebellar circuit

Population code for image motion

Preliminary command for eye velocity

Motor command


How do we think about visual motor transformations in terms of neural circuits1

How do we think about visual-motor transformations in terms of neural circuits?

Parieto-ponto-cerebellar circuit

MT

Preliminary command for eye velocity

Motor command


What are we trying to explain the many features of the pursuit behavior3

What are we trying to explain -- the many features of the pursuit behavior.

  • Smooth eye movement persists without image motion.

  • Population decoding for visual-motor transformations (probably done at multiple levels)

  • On-line gain control

  • Target choice in real-world situations

  • Long-term adaptive changes (learning)


So far we ve treated pursuit as a negative feedback control system with velocity memory

So far, we’ve treated pursuit as a negative feedback control system with velocity memory

Feedforward Gain

retina

Next, I’ll show that the feedforward gain of pursuit is variable. Gain control is another feature of pursuit that we need to understand at the level of neural circuits.


Use of perturbations to probe the gain of visual motor transformations for pursuit

Use of perturbations to probe the gain of visual-motor transformations for pursuit

Target position

Research of Joshua Schwartz


Use of perturbations to probe the gain of visual motor transformations for pursuit1

Use of perturbations to probe the gain of visual-motor transformations for pursuit

Target position

Research of Joshua Schwartz


Use of perturbations to probe the gain of visual motor transformations for pursuit2

Use of perturbations to probe the gain of visual-motor transformations for pursuit

Target position

Research of Joshua Schwartz


Use of perturbations to probe the gain of visual motor transformations for pursuit3

Use of perturbations to probe the gain of visual-motor transformations for pursuit

Target position

Research of Joshua Schwartz


Perturbations cause large responses during pursuit the gain is set to high

Perturbations cause large responses during pursuit: the gain is set to “high”

During pursuit

During fixation


Perturbations cause small responses during fixation the gain is set to low

Perturbations cause small responses during fixation: the gain is set to “low”

During pursuit

During fixation


Pursuit is a negative feedback control system with a variable feedforward gain

Pursuit is a negative feedback control system with a variable feedforward gain

VariableGain

retina


How do we think about gain control in terms of neural circuits

How do we think about gain control in terms of neural circuits?

Parieto-ponto-cerebellar circuit

Gain control circuit

MT

?

Vector

averaging

Preliminary command for eye velocity

X

Motor command

Site of gain control


Stimulation in fpa evokes smooth eye movements

Stimulation in FPA evokes smooth eye movements


Stimulation of fpa enhances the response to a perturbation delivered during fixation

Stimulation of FPA enhances the response to a perturbation delivered during fixation


Enhancement is in the direction of the perturbation not in the direction of the evoked eye movement

Enhancement is in the direction of the perturbation, not in the direction of the evoked eye movement


Enhancement is in the direction of the perturbation not in the direction of the evoked eye movement1

Enhancement is in the direction of the perturbation, not in the direction of the evoked eye movement


How do we think about gain control in terms of neural circuits1

How do we think about gain control in terms of neural circuits?

Parieto-frontal circuit

Parieto-ponto-cerebellar circuit

MT

Vector averaging

Frontal Pursuit Area

Preliminary command for eye velocity

X

Motor command

Site of gain control

What are the input signals that allow the frontal pursuit area to control the gain of the visual-motor transformation?


How do we think about gain control in terms of neural circuits2

How do we think about gain control in terms of neural circuits?

Parieto-frontal circuit

Parieto-ponto-cerebellar circuit

MT

Vector averaging

Frontal Pursuit Area

Preliminary command for eye velocity

X

Motor command

Site of gain control

Vision needs to be one input signal, since image motion has to turn the pursuit system on and initiate smooth tracking.


How do we think about gain control in terms of neural circuits3

How do we think about gain control in terms of neural circuits?

Parieto-frontal circuit

Parieto-ponto-cerebellar circuit

Feedback of motor command

MT

Vector averaging

Frontal Pursuit Area

Preliminary command for eye velocity

X

Motor command

Site of gain control

The frontal pursuit area needs to represent eye velocity as well as image velocity. (Note another positive feedback loop, like the one through the cerebellum)


Now we know why the fpa and cerebellum have very similar outputs during pursuit

Now we know why the FPA and cerebellum have very similar outputs during pursuit

FPA

Cerebellum


Now we know why the fpa and cerebellum have very similar outputs during pursuit1

Now we know why the FPA and cerebellum have very similar outputs during pursuit

FPA

Cerebellum

Uses image motion to initiate pursuit by increasing the internal gain of pursuit.

Uses eye velocity to keep the internal gain of pursuit high when image motion vanishes because of perfect tracking.

Uses image motion to initiate pursuit by driving eye acceleration.

Uses eye velocity to keep a moving eye moving when image motion vanishes because of perfect tracking.

Same basic signals, same basic positive feedback circuit, same basic goal of maintaining excellent tracking when the sensory input to the system goes away. Operating at very different levels of the motor hierarchy, one at a modulatory level, one at a nuts-and-bolts level.


What are we trying to explain the many features of the pursuit behavior4

What are we trying to explain -- the many features of the pursuit behavior.

  • Smooth eye movement persists without image motion.

  • Population decoding for visual-motor transformations (probably done at multiple levels)

  • On-line gain control

  • Target choice in real-world situations

  • Long-term adaptive changes (learning)


Anatomy of pursuit1

Anatomy of pursuit

Caudate

nucleus

How does it work when each part is doing the same neural computation?


Collaborators

Collaborators

Anne Churchland

Mark Churchland

Rich Krauzlis

Ed Morris

Nicholas Priebe

Joshua Schwartz

Leeland Stone

Masaki Tanaka

Albert Fuchs


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