brain imaging of motor learning - mcgill university · motor skill learning goals of this...

Brain Imaging of Motor LearningBrain Imaging of Motor LearningBrain Imaging of Motor Learning

Julien Doyon, Ph.D.Julien Doyon, Ph.D.ScientificScientific DirectorDirector

FunctionalFunctional NeuroimagingNeuroimaging UnitUnitUniversityUniversity of of MontrealMontreal GeriatricGeriatric InstituteInstitute

UniversityUniversity of of MontrealMontreal

CharacteristicsCharacteristics

ConceptualizedConceptualized as the acquisition of a as the acquisition of a specificspecific motormotor plan plan (or set) for the effective performance of an (or set) for the effective performance of an intendedintended action.action.

Acquisition Acquisition isis incrementalincremental.. MeasuredMeasured by a by a reductionreduction in in reactionreaction time and time and errorserrors, and/or , and/or

by a change in by a change in movementmovement synergysynergy and and kinematicskinematics.. Can Can bebe acquiredacquired eithereither explicitlyexplicitly or or implicitlyimplicitly.. ImplicitImplicit retrievalretrieval.. LongLong--lasting.lasting. DoesDoes not not dependdepend on on limbiclimbic structures.structures.

Motor Skill LearningMotor Skill Learning

CorticoCortico--StriatalStriatal SystemSystem

Carpenter, Core Text of Neuroanatomy, 2ème éd., 1982, Williams & Wilkins Company

VLoVLo

Dorsal and ventral premotor cortices


Supplementarymotor areas


Primary motorcortex

Primary motorcortex

StriatumStriatum

GlobuspallidusGlobuspallidus

CorticoCortico--CerebellarCerebellar SystemSystem

http://www.braincampus.com





Primary motorcortex

Primary motorcortex

VLc + VPLoVLc + VPLoXX

PonsPons

CerebellumCerebellum

HoshiHoshi et al., Nature vol8 (2005), 1491et al., Nature vol8 (2005), 1491--14931493

AnatomicalAnatomical Interactions Interactions BetweenBetween the the CorticoCortico--StriatalStriatal and and CorticoCortico--CerebellarCerebellar SystemsSystems


Motor, cognitive and physiological factorsMotor, cognitive and physiological factorsaffecting cerebral plasticity during motor learning :affecting cerebral plasticity during motor learning :

Learning phases: fast Learning phases: fast vsvs slow slow vsvs consolidation consolidation vsvsreconsolidation reconsolidation vsvs automatizationautomatization vsvs retention. retention.

Sleep, Nap, Interference. Sleep, Nap, Interference.

Type of motor learning: motor sequence Type of motor learning: motor sequence vsvs motor adaptation.motor adaptation.

Motor Learning:Motor Learning: Experimental ParadigmsExperimental ParadigmsMotor Sequence Learning Tasks: Motor Sequence Learning Tasks:

Incremental acquisition of a sequence of movements Incremental acquisition of a sequence of movements

4

32 1

Finger Sequence Task Serial Reaction Time Task

Motor Learning: Experimental ParadigmsMotor Learning: Experimental Paradigms

Visuomotor Adaptation: Kinematic

12

3

45

6

7

8

Targets appear in a random order:Inversed condition

requires

Motor Adaptation Tasks: Motor Adaptation Tasks: Capacity to compensate Capacity to compensate for environmental changesfor environmental changes

Force Field Adaptation: Dynamic


Goals of this presentationGoals of this presentation

To examine the cerebral plasticity mediating different phases ofTo examine the cerebral plasticity mediating different phases of motor motor sequence learning (MSL) and motor adaptation (MA) using sequence learning (MSL) and motor adaptation (MA) using fMRIfMRI..

To explore the To explore the behavioralbehavioral/functional determinants of cerebral plasticity /functional determinants of cerebral plasticity in both in both corticocortico--striatalstriatal (CS) and (CS) and corticocortico--cerebellarcerebellar (CC) systems.(CC) systems.

Contribution of sleep versus the simple passage of time to the Contribution of sleep versus the simple passage of time to the consolidation of motor memory tracesconsolidation of motor memory traces..

Neural substrates and physiological correlates mediating the Neural substrates and physiological correlates mediating the consolidation process of motor memory traces.consolidation process of motor memory traces.

Objective

To explore the To explore the dynamicdynamic cerebralcerebral changes changes thatthat occuroccur withinwithinthe striatum the striatum duringduring the the fastfast and slow phases of and slow phases of learninglearning of a of a sequencesequence of of movementsmovements, as , as wellwell as as afterafter performance has performance has becomebecome automatizedautomatized..

Motor Sequence Learning

Lehéricy et al., (2005), PNAS 102(35) 12566-71

Subjects : n = 14 (age: 19Subjects : n = 14 (age: 19--34, right handed)34, right handed) Task : Finger sequence task: 4Task : Finger sequence task: 4--keys response boxkeys response box

2 sequences to learn (Trained & Untrained) 2 sequences to learn (Trained & Untrained) 8 moves using 4 fingers (left hand)8 moves using 4 fingers (left hand)

Block design :Block design :

Scanning : 5 sessionsScanning : 5 sessions

Method

TR: 4.5 sTE: 40 ms: 90°bandwidth: 1562Hz/pixel FOV: 192 x 192 mm²matrix size: 128 x 128voxel size: 1.5 x 1.5 x 2.5 mm3

Practice done every day for a month

5 speed tests performed weekly, as well as before and after each scanning session (T1-T3, T4, T5)

PlasticityPlasticity WithinWithin the Striatum the Striatum DuringDuring MotorMotorSequenceSequence LearningLearning


Behavioral resultsBehavioral results



Imaging resultsImaging results



Imaging resultsImaging results

PlasticityPlasticity WithinWithin the the CerebellumCerebellum DuringDuringMotorMotor SequenceSequence LearningLearning


Objective

To explore the To explore the cerebralcerebral changes changes associatedassociated withwith the the earlyearlyand and automatizationautomatization phases of an phases of an adaptedadapted movementmovement..

Motor Adaptation

Doyon et al., Behav. Brain Res., 2009

Motor Adaptation: Motor Adaptation: Early Early vsvs AutomatizedAutomatized PhasePhase

1

2

3

4

5

6

7

8

Targets appear in a random order:Inversed condition

Motor Adaptation: Inversed Condition

requires

Targets appear in a random order:Direct condition

Control Condition: Direct Condition

1

2

3

4

5

6

7

8

requires


Motor Adaptation: Motor Adaptation: Early Early vsvs AutomatizedAutomatized PhasePhase

TasksTasksPrimary task:Primary task: Inversed mode (motor Inversed mode (motor

adaptation)adaptation) Direct mode (control)Direct mode (control)

Secondary task:Secondary task: Tone discrimination taskTone discrimination task

Dual tasks:Dual tasks: Inversed mode & tone Inversed mode & tone

discrimination task discrimination task simultaneouslysimultaneously


Motor Adaptation: Fast Motor Adaptation: Fast vsvs Automatic PhaseAutomatic PhaseExperimental ParadigmExperimental Paradigm

Day 1: Days 2 to 30 :15min/day

Day 26On avg.

Intro+ fMRI

Daily PracticeSessions on Tasks

fMRI

EarlyLearning

Extended Practice(subject tailored)

AutomaticExecution


Motor adaptation: Motor adaptation: AutomatizationAutomatization

Behavioral results


Motor adaptation: AutomatizationMotor adaptation: Automatization

Early IM – Early DM



Automatic IM – Automatic DM



(Automatic IM – Automatic DM) – (Early IM – Early DM)


Neural Substrates of Motor LearningNeural Substrates of Motor Learning

Motor sequencelearning

Motor adaptation

Fast

Lear

ning

Cognitiveprocesses

Cognitiveprocesses

Doyon & Benali (2005), Current Opinion Neurobiology

Motor cortical regions Parietal Cortices

Associative striatum Cerebellar cortices

Frontal associative regions

Sensorimotor striatum Cerebellar cortices and nuclei

Medial temporal lobe (hippocampus)

Consolidation

Fast

Lear

ning


Motor adaptation

Cognitiveprocesses

Cognitiveprocesses

Slow

Lear

ning

Motor cortical regions

Striatum CerebellumParietal cortex








Automatization

Slow

Lea

rnin

gNeural Substrates of Motor LearningNeural Substrates of Motor Learning

Fast

Lear

ning

Cerebellum


StriatumParietal cortex

Motor cortical regionsParietal cortex

Motor cortical regionsStriatum Cerebellum

Consolidation


Motor adaptation

Cognitiveprocesses

Cognitiveprocesses

Parietal cortex







Rete

ntio

nNeural Substrates of Motor LearningNeural Substrates of Motor Learning

Cerebellum

Motor cortical regionsMotor cortical regions

StriatumParietal cortex Parietal cortex

Fast

Lear

ning

Slow

Lear

ning

Time delay

CerebellumMotor cortical regionsMotor cortical regions

StriatumParietal cortex Parietal cortex

Automatization


Consolidation


Motor adaptation

Cognitiveprocesses

Cognitiveprocesses

Parietal cortex







Objective

To To dissociatedissociate betweenbetween the neural the neural substratessubstrates mediatingmediating motormotorsequencesequence learninglearning per seper se, versus performance (speed) of , versus performance (speed) of movementsmovements..

Dissociating Functional Brain Areas UnderlyingMotor Sequence Learning Versus its Expression

Pierre Orban, Philippe Peigneux,Pierre Maquet, Julien Doyon

Orban et al., 2010, NeuroImage

SeqLearn

55--elementelement fingerfingersequencesequence (2 1 3 4 1)(2 1 3 4 1)

NoSeq/Ctrl

FingerFinger tappingtapping(1, 2, 3 or 4 / (1, 2, 3 or 4 / slow, medium, slow, medium, fastfast rate)rate)

--12 blocks12 blocks

--LeftLeft hand hand movementsmovements

--Nb of Nb of movementsmovements: : 50/block50/block

Parametric fMRI design

1st level – FFX – effects of parametric modulation for each condition separately

2nd level – RFX – conjunction and between-condition subtractions

Significance: p < 0.001 (uncorrected)

Time

Experimental Design

3T fMRI study, block design, 32 subjects.

AutomatizedAutomatized sequencesequence(4 3 2 1) (4 3 2 1) atat slow, slow, medium and medium and fastfast raterate

Seq/Ctrl



SequenceLearning:SeqLearn

AutomatizedSequence:

Seq/CtrlFinger tapping

NoSeq/Ctrl

1 12 1 16 1 32

Hz Hz Hz Hz

Conditions



ResultsResults: : fMRIfMRI((ParametricParametric analyses)analyses)

FingerFinger tappingtapping((NoSeqNoSeq/Ctrl)/Ctrl)

AutomatizedAutomatizedSequenceSequence(4321)(4321)((SeqSeq/Ctrl)/Ctrl)

SequenceSequenceLearningLearning((SeqLearnSeqLearn))



ResultsResults: : fMRIfMRI(Conjonctions &(Conjonctions &ContrastContrastanalyses)analyses)

SeqLearnSeqLearn ∩∩SeqSeq/Ctrl/Ctrl ∩∩NoSeqNoSeq/Ctrl/Ctrl

SeqLearnSeqLearn ∩∩SeqSeq/Ctrl/Ctrl

SeqLearnSeqLearn ––SeqSeq/Ctrl/Ctrl



ObjectiveObjective

To To identifyidentify brainbrain regionsregions mediatingmediating the changes in the changes in movementmovement kinematicskinematics (i.e., transitions, (i.e., transitions, velocityvelocity) ) associatedassociatedwithwith the the learninglearning of a new of a new sequencesequence of of movementsmovements..

Cerebral Correlates of Movement KinematicChanges Related to Motor Sequence Learning

Pierre Orban, Philippe Peigneux, Marc Barakat, Pierre Maquet, Julien Doyon

Montreal, Canada and Liège, Belgium

Orban et al., Submitted, Eur. J. Neurosci.

MethodMethod• 12 right-handed subjects (6 males,

mean age = 26.5 years).

• Explicitly known 8-element sequence.

• Event-related fMRI design.

• 60 trials with left hand interspersedwith rest epochs (mean duration = 12s).

• Finger movements recorded using acustom-made MR compatible keypad.

• Output data: % of maximumdisplacement reflecting the position of each button as a function of time(sampling rate = 400 Hz).

• 3T MRI scanner (Magnetom Tim Trio,Siemens). (TR = 1000ms, voxel size =3.4 X 3.4 X 7 mm3, 16 slices).

CerebralCerebral CorrelatesCorrelates of of MovementMovement KinematicKinematicChanges Changes RelatedRelated to to MotorMotor SequenceSequence LearningLearning


CerebralCerebral CorrelatesCorrelates of of MovementMovement KinematicKinematic Changes Changes RelatedRelated to to MotorMotor SequenceSequence LearningLearning

Beh

avio

ralR

esul

ts


fMRI Data:Main Effect



fMRIData:

Vélocity

Transition

Vélocity/Transition



ConclusionsConclusionsConclusions

•• The lateral cerebellum (Lobule VI) and The lateral cerebellum (Lobule VI) and putamenputamen((sensorimoteursensorimoteur) contribute critically to experience) contribute critically to experience--dependent dependent learning learning per seper se of a new motor sequence.of a new motor sequence.

•• Activity in the lateral cerebellum and Activity in the lateral cerebellum and putamenputamen is mainly is mainly associated with improvement in finger movement transitions (coassociated with improvement in finger movement transitions (co--articulation, chunking).articulation, chunking).

CerebralCerebral PlasticityPlasticity AssociatedAssociated withwithMotorMotor SequenceSequence LearningLearning

Motor Motor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects,,Neural Neural SubstratesSubstrates and and PhysiologicalPhysiological CorrelatesCorrelates

…the memory of a given motor experience is thought to be dynamically re-processed off-line in a time-dependent fashion and transformed into an enduring state.

MotorMotor Memory ConsolidationMemory Consolidation

ParametricParametric design:design:

SpontaneousSpontaneous delayeddelayed gains in performance gains in performance withoutwithoutadditionaladditional practice practice followingfollowing an initial training session.an initial training session.

InterferenceInterference design:design:

TimeTime--dependentdependent reductionreduction in in interference from a interference from a competing task. competing task.

Walker et al., Walker et al., NeuronNeuron vol35 (2002), 205vol35 (2002), 205--211211

MotorMotor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects??

Walker et al., Walker et al., NeuronNeuron Vol. 35 (2002), 205Vol. 35 (2002), 205--211211


Sleep Contribution to Motor Memory Sleep Contribution to Motor Memory ConsolidationConsolidation

Remaining Issues:

• Nature of the motor tasks

• Neural substrates

• Stage(s) of sleep

Main Objectives:Main Objectives:

To study, through behavioral analyses, the effects ofTo study, through behavioral analyses, the effects ofsleep versus simple passage of time on the consolidationsleep versus simple passage of time on the consolidationof motor sequence learning or motor adaptation tasks.of motor sequence learning or motor adaptation tasks.

To identify, through To identify, through fMRIfMRI studies, the neural substrates studies, the neural substrates mediating the consolidation of both motor sequence andmediating the consolidation of both motor sequence andmotor adaptation.motor adaptation.

To To identifyidentify, , withwith polysomnographicpolysomnographic recordingsrecordings, the , the sleepsleepfeaturefeature(s) (s) involvedinvolved in the in the motormotor memorymemory consolidation.consolidation.

Sleep Contribution to Motor Memory Sleep Contribution to Motor Memory ConsolidationConsolidation

Experimental design:ExperimentalExperimental design:design:

Retest (12 h after initial training)

orSLEEPSLEEP

Trainingor


orSLEEPSLEEPPSG

Trainingor


or

PASSAGE OF PASSAGE OF TIME TIME ((withoutwithout napsnaps))

Training

or


or

PASSAGE OF TIME ((without naps

PASSAGE OF TIME without naps))

Training

or

4321

NIGHT group (n=26)NIGHT group (n=26)

DAY group (n=25)DAY group (n=25)

EveningEvening MorningMorning (2 h (2 h afterafter

awakeningawakening ))

4321

4321

4321

MorningMorning (2 h (2 h afterafter EveningEvening

awakeningawakening ) )

12 12 hourshours

12 12 hourshours

Motor Memory Consolidation: Sleep Motor Memory Consolidation: Sleep vs.vs.Simple Passage of Time Simple Passage of Time -- Behavioral StudyBehavioral Study

Doyon et al., 2009, Exp. Brain Res.

Behavioral Results: Motor Adaptation TaskBehavioral Results: Motor Adaptation TaskBehavioral Results: Motor Adaptation Task

Motor Memory Consolidation: Sleep Motor Memory Consolidation: Sleep vs.vs.Simple Passage of TimeSimple Passage of Time

0,84

0,85

0,86

0,87

0,88

0,89

0,9

Post-training Retest Post-training Retest

PI-S

peed

and

pre

cisi

on

SLEEP

PASSAGE

OF

TIME

significant +2% significant +2.5%

ANOVA 2 sessions X 2 groups= significant session effect:F(1, 24)=27,779, p=0,00002


Behavioral Results: Sequence TaskBehavioral Results: Sequence TaskBehavioral Results: Sequence Task

Fig.1. No significant difference in learning was observed between subjects trained in the morning (DAY group) or in the evening (NIGHT group).

Fig. 2. In the SEQ task, only the NIGHT group showed significant spontaneous delayed gains at retest in terms of the number of correct sequences produced in 30-sec trials.

Motor Memory Consolidation: Sleep Motor Memory Consolidation: Sleep vs.vs.Simple Passage of Time Simple Passage of Time –– Behavioral StudyBehavioral Study

18

19

20

21

22

23

24

Post-training Retest Post-training RetestSp

eed

(# s

eque

nces

per

30s

)

SLEEP

PASSAGE

OF

TIME

Significant + 14% Non-significant + 2%

ANOVA 2 sessions X 2 groups = significant interaction effect: F(1, 23)=10,362 p=0,0038

6

12

18

24

30

1 2 3 4 5 6 7 8 9 10 11 12 1 2 3

Spee

d (#

seq

uenc

es p

er 3

0s)

NIGHT groupDAY group

SLEEP

OR

PASSAGE

OF

TIME

Blocks of trials Retest 12h later


Motor Sequence Learning: “Nap Effects”Motor Sequence Learning: Motor Sequence Learning: ““Nap EffectsNap Effects””

4

321

0

20

40

60

80

100

120

% im

prov

emen

t

0hPost-Test 8hPost-Test 22hPost-TestPre-Test

nap night sleepN=6nap

(90 min)


Korman et al., 2007, Nat. Neurosci.; Doyon et al., 2009, Exp. Brain Res.

Polysomnographic findings

Morin et al., 2008, Sleep

MotorMotor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects

Fast Spindles (13-15 Hz)

0

0.5

1

1.5

2

2.5

3

3.5

F3 F4 Fz C3 C4 Cz P3 P4 Pz O1 O2 Oz F3 F4 Fz C3 C4 Cz P3 P4 Pz O1 O2 Oz

SEQ ADPT

dens

ite fu

seau

x ra

pide

sN

b to

tal f

usea

ux/D

urée

NR

EM

SEQ

CTRL Seq

ADPT

CTRL Adpt* * * *

*


Slow spindles (11-13 Hz)

0

0.5

1

1.5

2

2.5

3

3.5

F3 F4 Fz C3 C4 Cz P3 P4 Pz O1 O2 Oz F3 F4 Fz C3 C4 Cz P3 P4 Pz O1 O2 Oz

SEQ ADPT

dens

ite fu

seau

x le

nts

Nb

tota

l fus

eaux

/Dur

ée N

RE

M

SEQ

CTRL Seq

ADPT

CTRL Adpt


Neuronal Neuronal SubstratesSubstrates AssociatedAssociatedwithwith Consolidation of a Consolidation of a MotorMotor

Memory Trace:Memory Trace:MotorMotor SequencSequenc LearningLearning


Automatization

Slow

Lea

rnin

gFa

stLe

arni

ng

Cerebellum


StriatumParietal cortex

Motor cortical regionsParietal cortex


Consolidation


Motor adaptation

Cognitiveprocesses

Cognitiveprocesses

Parietal cortex







Experimental design:ExperimentalExperimental design:design:

Neural Substrates of Motor Memory ConsolidationNeural Substrates of Motor Memory Consolidation

PolysomnographicRecordings

Debas et al., Submitted

BehavioralBehavioral ResultsResults: : MotorMotor SequenceSequence TaskTask

*p=.03



y = -30

Motor cortex

y = -56

Cerebellum: V, VI, VIII

y = 8

Putamen/GlobusPallidus

fMRI Results: Motor Sequence Task:Activated Areas Common to both Night and Day Groups.fMRIfMRI ResultsResults: : MotorMotor SequenceSequence TaskTask::ActivatedActivated Areas Common to Areas Common to bothboth Night and Day Groups.Night and Day Groups.

Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Conjunction Analysis: Immediate PostConjunction Analysis: Immediate Post--TrainingTraining


Bilateral Putamen

y = - 5

Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Contrast Analysis: Retest SessionContrast Analysis: Retest Session

fMRI Results: Motor Sequence Task:Night > Day Group.fMRIfMRI ResultsResults: : MotorMotor SequenceSequence TaskTask::Night Night >> Day Group.Day Group.


Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Group x Session InteractionGroup x Session Interaction

fMRI Results: Motor Sequence Task:

Group (Night vs Day) bySession (Retest vs Immediate Post-training)

fMRIfMRI ResultsResults: : MotorMotor SequenceSequence TaskTask::

Group (Night vs Day) byGroup (Night vs Day) bySession (Session (RetestRetest vs vs ImmediateImmediate PostPost--training)training)



Identification of Identification of functional networks in functional networks in fMRIfMRI data using spatial data using spatial independent component analysis (ICA).independent component analysis (ICA).

Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Connectivity and Integration AnalysesConnectivity and Integration Analyses

Selection of several regions of interest (Selection of several regions of interest (ROIsROIs) used for the ) used for the connectivity analyses connectivity analyses


Correlations between ROIS for the two groups (Day and Night) durCorrelations between ROIS for the two groups (Day and Night) during the ing the ““testtest”” and and ““retestretest”” scanning sessions scanning sessions


Jour - Test Jour – Re-test

Nuit - Test Nuit – Re-test

6262

ConnectivityConnectivity and and IntegrationIntegrationof of MotorMotor Networks: Networks: MethodMethod

SelectionSelection of ROIof ROI Spatial Independent Spatial Independent

Component Component AnalysisAnalysis 11

UsedUsed a a motormotor network network presentpresentin all participantsin all participants

Identification of 2 Identification of 2 subsub--networks (networks (AssocAssoc., ., SensoriSensori.) .) ((CoynelCoynel et al., 2010)et al., 2010)

WithinWithin and and betweenbetweennetworks networks functionalfunctionalconnectivityconnectivity quantification quantification HierarchicalHierarchical integrationintegration Covariance Covariance betweenbetween ROIROI’’ss

BOLD time coursesBOLD time courses

M

A

B

1 Perlbarg et al., ISBI 2008 & HBM 2009 2 Marrelec et al., Med Im An 2008 CoynelCoynel et al., In et al., In presspress, , NeuroImageNeuroImage

Changes in Functional Integration Following Changes in Functional Integration Following Consolidation of Motor Sequence LearningConsolidation of Motor Sequence Learning

Debas et al., OHBM, 2010

MotorMotor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects

Spindles detection: an Spindles detection: an automatic algorithm was used to automatic algorithm was used to detect amplitude, duration and number of fast (13.1detect amplitude, duration and number of fast (13.1--14.9 14.9 Hz) and slow (11.1Hz) and slow (11.1--12.9 Hz) spindles on frontal (F3, 12.9 Hz) spindles on frontal (F3, FzFz, , F4), central (C3, F4), central (C3, CzCz, C4) and parietal (P3, , C4) and parietal (P3, PzPz, P4) , P4) derivations during the NREM sleep.derivations during the NREM sleep.

BOLD activity: based on the results of the BOLD activity: based on the results of the fMRIfMRI analysis, analysis, parameter estimates (beta values) for significant parameter estimates (beta values) for significant voxelsvoxels in in both the right and the left both the right and the left putamenputamen were extracted for were extracted for every subject of the Night/sleep group.every subject of the Night/sleep group.

Statistical analysis: Pearson productStatistical analysis: Pearson product--moment correlations moment correlations were carried out between sleep spindles, changes in BOLD were carried out between sleep spindles, changes in BOLD activity in both activity in both putamenputamen and overnight gains in and overnight gains in performance.performance.

Barakat et al., In preparation

Slow spindles amplitudeSlow spindles amplitude

Significant correlations with BOLD changes in the right putamen

Significant correlations with both BOLD changes in the right putamen and gains in performance

Fast spindles amplitudeFast spindles amplitude

Significant correlations with BOLD changes in the right putamen

Significant correlation with both BOLD changes in the right putamen and gains in performance

Neuronal Neuronal SubstratesSubstrates AssociatedAssociatedwithwith Consolidation of a Consolidation of a MotorMotor

Memory Trace:Memory Trace:MotorMotor AdaptationAdaptation

No difference between Day and Night GroupsSession by Blocks: (p = .034)

50

100

150

200

250

300

0 10 20 30 40 50 60

Test

Retest

Trials

First 4 blocks

BehavioralBehavioral ResultsResults: : MotorMotor Adaptation Adaptation TaskTask


X = -27

Motor cortex Cerebellum: V, VI, VIII

X = 0

y = -60

fMRI Results: Motor Adaptation Task:Activated Areas Common to both Night and Day Groups.fMRIfMRI ResultsResults: : MotorMotor Adaptation Adaptation TaskTask::ActivatedActivated Areas Common to Areas Common to bothboth Night and Day Groups.Night and Day Groups.

Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Conjunction Analysis: Immediate PostConjunction Analysis: Immediate Post--TrainingTraining

fMRIfMRI ResultsResults: : MotorMotor Adaptation Adaptation TaskTask::At Retest: The Night group did not differ from the Day group.At Retest: The Night group did not differ from the Day group.Conjunction analysis: Both groups Conjunction analysis: Both groups showdedshowded greater activity in the greater activity in the cerebellum at retest than during the immediate testing session.cerebellum at retest than during the immediate testing session.

Y = -72 SVC 0f 10mm: p = .05 FWE corr.

Cerebellum: Lobule VI

Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Conjunction Analysis: Retest Conjunction Analysis: Retest vsvs Immediate PostImmediate Post--TrainingTraining

Amount of saving between the two sessions (%)

Cer

ebel

lar (

L.V

I) B

OLD

resp

onse

X = 36

SVC of 10mm: p = .005 FWE corr.

-15

-10

-5

0

5

10

-60 -40 -20 0 20 40 60

fMRI Results: Motor Adaptation Task:

• The amount of savings correlate with activityin ipsilateral Cerebellum (Lobule VI).

fMRIfMRI ResultsResults: : MotorMotor Adaptation Adaptation TaskTask::

•• The The amountamount of of savingssavings correlatecorrelate withwith activityactivityin in ipsilateralipsilateral CerebellumCerebellum (Lobule VI).(Lobule VI).

Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Correlation Analysis:Correlation Analysis:

ConclusionsConclusions• Sleep contributes to the consolidation process of a new motor sequencelearning task, while the simple passage of time is sufficient to produce a similar effect when using a motor adaptation paradigm.

• The striatum (and the putamen in particular) is involved in the off-line, sleep-dependent, consolidation process of a newly learned motor sequence.

• By contrast, the cerebellum plays a critical role in the consolidation of a new internal model adapted to task demands.

• For the first time, we demonstrate that the amplitude of both fast and slow sleep spindles correlates with previously demonstrated changes of activity in the putamen after motor consolidation, and with behavioural gains of performance in motor sequence learning.

Motor Memory Consolidation: Sleep Motor Memory Consolidation: Sleep vs.vs.Simple Passage of TimeSimple Passage of Time

AcknowledgementsAcknowledgements

University of Montreal

Julie CarrierJulie CarrierRick Rick HogeHoge

Marc Marc BarakatBarakatKaren Karen DebasDebasPierre Pierre OrbanOrbanGeneviGenevièève Albouyve AlbouyOvidiuOvidiu LunguLunguStuart Stuart FogelFogelSSéébastien bastien ProulxProulxSamuel Samuel LaventureLaventure

Research associate

Vo An NguyenVo An Nguyen

INSERM / U678, Paris

HabibHabib BenaliBenaliStStééphane phane LehLehééricyricyGuillaume Guillaume MarrelecMarrelec

Haifa University, Israël

AviAvi KarniKarniMaria Maria kormankorman

University of Liège, Belgium

Pierre MaquetPierre MaquetPhilippe Philippe PeigneuxPeigneux

brain imaging of motor learning - mcgill university · motor skill learning goals of this...

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