Post on 08-Aug-2020
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
Dorsal and ventral premotor cortices
Supplementarymotor areas
Supplementarymotor areas
Primary motorcortex
Primary motorcortex
StriatumStriatum
GlobuspallidusGlobuspallidus
CorticoCortico--CerebellarCerebellar SystemSystem
http://www.braincampus.com
Dorsal and ventral premotor cortices
Dorsal and ventral premotor cortices
Supplementarymotor areas
Supplementarymotor areas
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 Skill LearningMotor Skill Learning
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
Motor Skill LearningMotor Skill Learning
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
Lehéricy et al., (2005), PNAS 102(35) 12566-71
Behavioral resultsBehavioral results
PlasticityPlasticity WithinWithin the Striatum the Striatum DuringDuring MotorMotorSequenceSequence LearningLearning
Lehéricy et al., (2005), PNAS 102(35) 12566-71
Imaging resultsImaging results
PlasticityPlasticity WithinWithin the Striatum the Striatum DuringDuring MotorMotorSequenceSequence LearningLearning
Lehéricy et al., (2005), PNAS 102(35) 12566-71
Imaging resultsImaging results
PlasticityPlasticity WithinWithin the the CerebellumCerebellum DuringDuringMotorMotor SequenceSequence LearningLearning
Lehéricy et al., (2005), PNAS 102(35) 12566-71
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
Doyon et al., Behav. Brain Res., 2009
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
Doyon et al., Behav. Brain Res., 2009
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
Doyon et al., Behav. Brain Res., 2009
Motor adaptation: Motor adaptation: AutomatizationAutomatization
Behavioral results
Doyon et al., Behav. Brain Res., 2009
Motor adaptation: AutomatizationMotor adaptation: Automatization
Early IM – Early DM
Doyon et al., Behav. Brain Res., 2009
Motor adaptation: AutomatizationMotor adaptation: Automatization
Automatic IM – Automatic DM
Doyon et al., Behav. Brain Res., 2009
Motor adaptation: AutomatizationMotor adaptation: Automatization
(Automatic IM – Automatic DM) – (Early IM – Early DM)
Doyon et al., Behav. Brain Res., 2009
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 sequencelearning
Motor adaptation
Cognitiveprocesses
Cognitiveprocesses
Slow
Lear
ning
Motor cortical regions
Striatum CerebellumParietal cortex
Neural Substrates of Motor LearningNeural Substrates of Motor Learning
Motor cortical regions Parietal Cortices
Associative striatum Cerebellar cortices
Frontal associative regions
Sensorimotor striatum Cerebellar cortices and nuclei
Medial temporal lobe (hippocampus)
Doyon & Benali (2005), Current Opinion Neurobiology
Automatization
Slow
Lea
rnin
gNeural Substrates of Motor LearningNeural Substrates of Motor Learning
Fast
Lear
ning
Cerebellum
Motor cortical regions
StriatumParietal cortex
Motor cortical regionsParietal cortex
Motor cortical regionsStriatum Cerebellum
Consolidation
Motor sequencelearning
Motor adaptation
Cognitiveprocesses
Cognitiveprocesses
Parietal cortex
Motor cortical regions Parietal Cortices
Associative striatum Cerebellar cortices
Frontal associative regions
Sensorimotor striatum Cerebellar cortices and nuclei
Medial temporal lobe (hippocampus)
Doyon & Benali (2005), Current Opinion Neurobiology
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
Motor cortical regionsStriatum Cerebellum
Consolidation
Motor sequencelearning
Motor adaptation
Cognitiveprocesses
Cognitiveprocesses
Parietal cortex
Motor cortical regions Parietal Cortices
Associative striatum Cerebellar cortices
Frontal associative regions
Sensorimotor striatum Cerebellar cortices and nuclei
Medial temporal lobe (hippocampus)
Doyon & Benali (2005), Current Opinion Neurobiology
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
Dissociating Functional Brain Areas UnderlyingMotor Sequence Learning Versus its Expression
Orban et al., 2010, NeuroImage
SequenceLearning:SeqLearn
AutomatizedSequence:
Seq/CtrlFinger tapping
NoSeq/Ctrl
1 12 1 16 1 32
Hz Hz Hz Hz
Conditions
Dissociating Functional Brain Areas UnderlyingMotor Sequence Learning Versus its Expression
Orban et al., 2010, NeuroImage
ResultsResults: : fMRIfMRI((ParametricParametric analyses)analyses)
FingerFinger tappingtapping((NoSeqNoSeq/Ctrl)/Ctrl)
AutomatizedAutomatizedSequenceSequence(4321)(4321)((SeqSeq/Ctrl)/Ctrl)
SequenceSequenceLearningLearning((SeqLearnSeqLearn))
Dissociating Functional Brain Areas UnderlyingMotor Sequence Learning Versus its Expression
Orban et al., 2010, NeuroImage
ResultsResults: : fMRIfMRI(Conjonctions &(Conjonctions &ContrastContrastanalyses)analyses)
SeqLearnSeqLearn ∩∩SeqSeq/Ctrl/Ctrl ∩∩NoSeqNoSeq/Ctrl/Ctrl
SeqLearnSeqLearn ∩∩SeqSeq/Ctrl/Ctrl
SeqLearnSeqLearn ––SeqSeq/Ctrl/Ctrl
Dissociating Functional Brain Areas UnderlyingMotor Sequence Learning Versus its Expression
Orban et al., 2010, NeuroImage
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
Orban et al., Submitted, Eur. J. Neurosci.
CerebralCerebral CorrelatesCorrelates of of MovementMovement KinematicKinematic Changes Changes RelatedRelated to to MotorMotor SequenceSequence LearningLearning
Beh
avio
ralR
esul
ts
Orban et al., Submitted, Eur. J. Neurosci.
fMRI Data:Main Effect
Orban et al., Submitted, Eur. J. Neurosci.
CerebralCerebral CorrelatesCorrelates of of MovementMovement KinematicKinematic Changes Changes RelatedRelated to to MotorMotor SequenceSequence LearningLearning
fMRIData:
Vélocity
Transition
Vélocity/Transition
Orban et al., Submitted, Eur. J. Neurosci.
CerebralCerebral CorrelatesCorrelates of of MovementMovement KinematicKinematic Changes Changes RelatedRelated to to MotorMotor SequenceSequence LearningLearning
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
MotorMotor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects??
Walker et al., Walker et al., NeuronNeuron Vol. 35 (2002), 205Vol. 35 (2002), 205--211211
MotorMotor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects??
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
Retest (12 h after initial training)
orSLEEPSLEEPPSG
Trainingor
Retest (12 h after initial training)
or
PASSAGE OF PASSAGE OF TIME TIME ((withoutwithout napsnaps))
Training
or
Retest (12 h after initial training)
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
Doyon et al., 2009, Exp. Brain Res.
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
Doyon et al., 2009, Exp. Brain Res.
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)
MotorMotor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects??
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* * * *
*
MotorMotor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects??
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
MotorMotor Memory Consolidation: Memory Consolidation: SleepSleep EffectsEffects??
Neuronal Neuronal SubstratesSubstrates AssociatedAssociatedwithwith Consolidation of a Consolidation of a MotorMotor
Memory Trace:Memory Trace:MotorMotor SequencSequenc LearningLearning
Neural Substrates of Motor LearningNeural Substrates of Motor Learning
Automatization
Slow
Lea
rnin
gFa
stLe
arni
ng
Cerebellum
Motor cortical regions
StriatumParietal cortex
Motor cortical regionsParietal cortex
Motor cortical regionsStriatum Cerebellum
Consolidation
Motor sequencelearning
Motor adaptation
Cognitiveprocesses
Cognitiveprocesses
Parietal cortex
Motor cortical regions Parietal Cortices
Associative striatum Cerebellar cortices
Frontal associative regions
Sensorimotor striatum Cerebellar cortices and nuclei
Medial temporal lobe (hippocampus)
Doyon & Benali (2005), Current Opinion Neurobiology
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
Neural Substrates of Motor Memory ConsolidationNeural Substrates of Motor Memory Consolidation
Debas et al., Submitted
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
Debas et al., Submitted
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.
Debas et al., Submitted
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)
Debas et al., Submitted
Debas et al., Submitted
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
Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Connectivity and Integration AnalysesConnectivity and Integration 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
Neural Substrates of Motor Memory Consolidation:Neural Substrates of Motor Memory Consolidation:Connectivity and Integration AnalysesConnectivity and Integration Analyses
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
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
Neural Substrates of Motor Memory ConsolidationNeural Substrates of Motor Memory Consolidation
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