FMRI studies of the human basal ganglia learning system
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FMRI studies of the human basal ganglia learning system
Carol A. SegerCognitive and Behavioral Neuroscience programs
Department of Psychology
Colorado State University
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W. W. Norton
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Memory and Habit
Habit: Slowly acquired associations between stimuli and responses/outcomes.
Memory: Memory for particular episodes
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Baited arm
Place learning: always go to the east arm (memory)
Response learning: always turn right (habit)
Training trials: Rat starts at S armProbe trials: Rat starts at N arm
N
W E
Packard & McGaugh, 1996
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placeresponse
place 11 2response 1 10
Caudate Hippocampal
Did injections of lidocaine to temporarily deactivate area.
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Caudate Nucleus / Basal Ganglia
Basal ganglia: Caudate Putamen Globus Pallidus
Caudate and Putamen together are known as the striatum
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SMA/PMCSSC
Motor
GP / SN
thalamus
DLPFCParietal
Spatial or Cognitive
GP / SN
thalamus
Visual
GP / SN
thalamus
Affective
GP / SN
thalamus
Putamen Head of caudate
Tail ofcaudate
VentralStriatum /NA
VLPFCInf tempSup temp
OFC, cinghipp, amg
Cortico-striatal processing loops
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Striatal learning in humans
Problem: Humans use the medial temporal lobe memory system for tasks that other animals learn using the striatal system.
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Probabilistic Classification
Task View set of cards Decide if the cards indicate “rain” or “shine”
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Category Structure Cues P(pattern) P(rain)0 0 0 0 ---- ----0 0 0 1 0.140 0.150 0 1 0 0.084 0.380 0 1 1 0.087 0.100 1 0 0 0.084 0.620 1 0 1 0.064 0.180 1 1 0 0.047 0.500 1 1 1 0.041 0.211 0 0 0 0.140 0.851 0 0 1 0.058 0.501 0 1 0 0.064 0.821 0 1 1 0.032 0.431 1 0 0 0.087 0.901 1 0 1 0.032 0.571 1 1 0 0.041 0.791 1 1 1 ---- ----
76% 56% 43% 24%Cue Strength
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Amnesia
Amnesics are not impaired for 1st 50 trials.
Knowlton, Gluck & Squire, 1994Knowlton, Gluck & Squire, 1994
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Huntington’s disease
Damage to the striatum
Impaired on probabilistic classification
A possible human correlate of habit learning.
Knowlton et al. 1996Knowlton et al. 1996
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Methods
BaselinePredict Predict Baseline
Alternated blocks of prediction and baseline trials.4 scans total24 prediction trials per scanParticipants:8 right-handed, fluent English speakers
Predict • • •
Poldrack, R. A., Prabhakaran, V., Seger, C. A., & Gabrieli, J. D. E. (1999). Striatal activation during cognitive skill learning. Neuropsychology, 13, 564-574.
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Weather Prediction: Behavior
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Probabilistic Classification Task:Classification > Baseline
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Basal ganglia and hippocampus
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S1 S2 S3 S4
Right caudate(head)
R medialtemporal
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Competition between MTL and striatal learning systems
Poldrack et al. 2001
Probabilistic classification task (yellow, triangles)Paired associates task (blue, circles)
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Outstanding questions
Reason for recruitment of striatum Actual engram location? Executive functioning?
• Feedback
• Uncertainty / Probabilistic nature of task Modulatory system related to reward?
Nature of competition between MTL and striatal learning systems
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Study 1: Feedback and Stimulus - outcome contingencies
Manipulate degree of probabilistic relationships from deterministic to random
Examine negative vs. positive feedback. Requires a post hoc analysis, which is possible due to the event related design.
Examine basal ganglia and medial temporal lobe interrelationships
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Trial procedure
Correct0 ms
2500 ms…
3500 ms
3000 ms
While stimulus is on the screen, participants press key for rain or sun
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Stimulus - outcome relationships
Stimulus Relationship P ( rain)1 Deterministic 1002 Deterministic 03 Probabilistic 904 Probabilistic 105 Probabilistic 806 Probabilistic 207 Random 508 Random 50
Baseline NA
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Participants: 15 young adults Conditions analyzed
Stimulus type• Det, Prob, Ran
Correctness• C and I
Feedback received• P and N
Examples• Det-CP Det-IN• Ran-P Ran-N• Prob-CP Prob-IN Prob-CN• Baseline
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Comparisons
Areas associated with classification: Conjunction analysis Det-CP > baseline and Prob-CP > baseline
Areas associated with processing feedback: Ran-P < > Ran-N Prob-CP < > Prob-CN
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Learning across blocks
1 2 3 Block
% correct
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DeterministicProbabilisticRandom
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Det-CPProb-CPBaseline
Right body / tail caudate
1 2 3 Block
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Det-CPProb-CPBaseline
1 2 3 Block
% signalchange
Left body / tail caudate
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Successful classification versusBaseline(Det-CP > base) and (Prob-CP > base)
Z = 19
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Areas associated with feedback: Head of the caudate
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Z = 19
Prob-CN >Prob-IN
Ran-P > Ran-N
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Interrelationships between hippocampal and caudate activity
Ran-P > Ran-N Det-CP HippocampusRight caudate .47 #Left caudate .63 *
Prob-CPRight caudate .00Left caudate .04
Ran-P:Right caudate .33Left caudate -.10
#: p < .1; *: p < .05
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Right caudate-B1 Left caudate-B1Accuracy .61 * .57 *
Correlations between blood flow and successful learning
Right hippocampusAccuracy-B1 -.59 *
*: p < .05
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Study 2: Observational and Feedback learning
Basal ganglia play important role in learning via feedback Feedback leads to better learning than observe
in normal subjects on complex categorization tasks.
Learning via feedback is impaired in PD Could be due to the DA reward circuits in the
basal ganglia.
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Stimulus set 1 (length-angle)
Category A Category B
Baseline
Ashby, Maddox, & Bohil (2002)
Category A Category B
Baseline
Set 2: Length-width
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Observational Learning
B
500 ms
250 ms
2500 msXXXXX
500 ms
250 ms
250 ms
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Feedback Learning
F
500 ms
250 ms
2500 msCorrect
500 ms
250 ms
250 ms
Training portion
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Test trials: Observe and Feedback
T
500 ms
250 ms
2500 msXXXXX
500 ms
250 ms
250 ms
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Methods
12 participants Within subjects design: Each participant did
both observe and feedback, counterbalanced, with different stimulus set.
Block design Alternated task blocks with baseline blocks Every 6th task block was a test block.
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Classification performance on test trials
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Observe Feedback
PercentageCorrect
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Common classification activity: body and tail of caudate.
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Obs > Base Feed C > base
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Head of caudate
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Obs Obs- Base- Feed Feed- Base- test Obs test Feed
PercentSignal change
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Hippocampus / MTL
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Obs > Base
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Feed C > Base
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Tentative conclusions from in-progress studies
Role of the head of the caudate differs from that of the body/tail of the caudate Tail-body: stimulus-outcome mapping.
• Consistent with the “visual” corticostriatal loop Head: related to processing feedback,
expectancy, executive functioning.• Consistent with the “cognitive” corticostriatal loop
Hippocampal - striatal antagonism not straightforward
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