cerebellumlecture haith 2017€¦ · cerebellum’is’required’to’learn novel’coordination...
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Forward models in the cerebellum: Predicting, Planning, Learning
Adrian Haith, PhDAssistant Professor, Department of Neurology
Johns Hopkins University
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Forward ModelsKnowing the state of the body is critical for accurate movementBut: long (~100ms) delays in receiving sensory feedback
Solution: Forward Model
• Simulates consequences of motor commands
• Predicts future state of the body
• Believed to be a primary function of the cerebellum
Forward Model
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Uses of Forward Models
• Potential uses of forward models:– Forward models provide an alternative estimateof the state of the body during active movement
– This should enable rapid compensation for erratic motor commands
– Forward models allow one to plan appropriate movements to achieve desired goals
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Moving without a forward model
• Cerebellar ataxia
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Forward models improve proprioception
Passive Movement by robot
Active Movement(stopped by a virtual wall)
Report PercievedLimb Position
(Cerebellar Ataxia)
(Estimation Varia
bility)
Bhanpuri et al., 2013
Integrating knowledge of motor commands improves perception in controls but not cerebellar patients
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Control
Role of forward models in feedback control• Our motor commands are always variable– Knowledge of bad motor commands can be used to correct an errant movement online
Example: Saccades
Xu-‐Wilson et al., 2009
Cerebellar
Compensation for slow start absent in patients
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If cerebellum really implements forward models, cerebellar output should resemble movement outcomes, not motor commands
Does appear to be the case for saccades:
Simple spike population response encodes impending velocity profile of a saccadeAlso some evidence for arm movements.
Encoding of eye kinematics in the cerebellum
Herzfeld et al., 2015
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Co-‐ordination versus prediction
Manipulating an object with both hands requires precise coordination
Common argument: Such coordination is enabled by forward models
Can easily co-‐ordinate effectors without having to do prediction
e.g. co-‐ordinatingeyelids while blinking!
Wolpert & Flanagan, 2001
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Coordination is not cerebellum-‐dependentUnloading
timeExternal Unloading
SelfUnloading
Anticipatory reduction of force
Diedrichsen et al., 2004
Healthy Controls
Intact in cerebellar patients
NB – colors here reflect unloading speed
Cerebellar Patients
Co-‐ordination Prediction
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Cerebellum is required to learn novel coordination
Participants taught a novel coordination pattern:Button-‐trigeredunloading
Diedrichsen et al., 2004
No learning in cerebellar patients
Downward acceleration in catch trials (surprise lack of unloading) -‐ LEARNING
Cerebellum does play a critical role in learning new patterns of coordination
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Visuomotor rotation
Adaptation
Cursor path rotated relative to hand
Force Field
Force field applied to the hand• Strength/direction of force
depends on hand position/speed
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Time course of adaptation
• Typically occurs in minutes• Stereotypical exponential learning curve:
• Characterizable through an error-‐driven learning rule:
𝑥"#$ = 𝐴𝑥" + 𝐵𝑒"
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Adaptation depends on the cerebellum
Maschke et al., 2004
• Healthy controls regain baseline levels of performance• Cerebellar patients never do
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Adaptation depends on the cerebellum
Another example:– Patients with severe cerebellar ataxia show limited adaptation
– Gradual introduction of perturbation enables learning
Criscimagna-‐Hemminger et al., 2010
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Adaptation is associated with altered prediction
Synofzik et al., 2008
Is adaptation mediated through a change in the cerebellar forward model?
Exposure to perturbation affects both movement andperception
Both effects blunted in cerebellar patients
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Adaptation is driven by sensory prediction errors
45 degree visuomotor rotation
Subset of subjects instructed how to “cheat”
Mazzoni & Krakauer, 2006
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Adaptation is driven by sensory prediction errors
Similar behavior also seen when throwing balls while wearing prism goggles
Martin et al., Brain, 1996
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No implicit recalibration in cerebellar patients
Taylor et al., 2010
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Multiple components of adaptation
• Not ALL adaptation is due to forward model recalibration
• At least two dissociable components of learning:
• Cerebellum believed to be responsible for slow, implicit component. What about other component?
Cerebellum
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Reaction Time and Motor Learning
• RT increases during motor adaptation:
Fernandez-‐Ruiz et al., 2011
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Reaction Time and Motor Learning
Haith et al., 2015
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Lowering RT limits expression of learning
Haith et al., 2015
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Reaction Time and Savings
Haith et al., 2015
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Reaction Time and SavingsDay-‐by-‐day comparison:
Haith et al., 2015
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Implicit vs Explicit learning
+=
Taylor et al., 2014
Adaptation composed of multiple components• Implicit recalibration (based
on forward model)• Explicit re-‐aiming
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Cerebellar damage impairs both implicit andimplicit learning
Same paradigm, in controls versus cerebellar patients
Butcher et al., In Prep
Controls
Patients
Net Learning
Re-‐Aiming Recalibration
+
=
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Beyond Adaptation• Cerebellum also critical for less structured forms of learning– Learning arbitrary associations between stimuli and actions
• Neuroimaging studies consistently implicate cerebellum
• Learning of arbitrary visuomotorassociations is impaired in individuals with cerebellar ataxia
Balsers & Ramnani, 2011
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De Novo Learning
• Is the cerebellum involved in ALL kinds of learning?– Probably not
“De novo” learning task-‐ Cannot be learned through adaptation of an existing controller
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De Novo Learning
• Is the cerebellum involved in ALL kinds of learning?– Probably not
“De novo” learning task-‐ Cannot be learned through adaptation of an existing controller
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De novo learning and the cerebellum
• Preliminary data suggest that learning of this kind is unaffected in patients with cerebellar ataxia
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Cerebellum and cognition
• Clear that cerebellum has role in cognitive functions
• Could some regions of the cerebellum implement models of the cortex, rather than the body?
CortexInput Output
PredictedOutput
• Could account for cerebellar role in “automation” of responses…
Cerebellum
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Summary• The cerebellum implements a forward model, predicting
the future state of the body based on current state and current motor commands
• Strong evidence that the output of a forward model influences the estimated state of the body
• Fair evidence that forward models also support movement planning
• The cerebellum likely does much more besides implement forward models– Many open questions!