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FMRI studies of the human basal ganglia learning system. Carol A. Seger Cognitive and Behavioral Neuroscience programs Department of Psychology Colorado State University. p.314. W. W. Norton. Memory and Habit. Habit: Slowly acquired associations between stimuli and responses/outcomes.
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FMRI studies of the human basal ganglia learning system Carol A. Seger Cognitive and Behavioral Neuroscience programs Department of Psychology Colorado State University
p.314 W. W. Norton
Memory and Habit • Habit: Slowly acquired associations between stimuli and responses/outcomes. • Memory: Memory for particular episodes
N W E Baited arm Place learning: always go to the east arm (memory) Response learning: always turn right (habit) Training trials: Rat starts at S arm Probe trials: Rat starts at N arm Packard & McGaugh, 1996
Caudate Nucleus / Basal Ganglia Basal ganglia: Caudate Putamen Globus Pallidus Caudate and Putamen together are known as the striatum
Motor Spatial or Cognitive Visual Affective VLPFC Inf temp Sup temp OFC, cing hipp, amg SMA/PMC SSC DLPFC Parietal Tail of caudate Head of caudate Ventral Striatum /NA Putamen GP / SN GP / SN GP / SN GP / SN thalamus thalamus thalamus thalamus Cortico-striatal processing loops
Striatal learning in humans • Problem: Humans use the medial temporal lobe memory system for tasks that other animals learn using the striatal system.
Probabilistic Classification • Task • View set of cards • Decide if the cards indicate “rain” or “shine”
Category Structure CuesP(pattern)P(rain) 0 0 0 0 ---- ---- 0 0 0 1 0.140 0.15 0 0 1 0 0.084 0.38 0 0 1 1 0.087 0.10 0 1 0 0 0.084 0.62 0 1 0 1 0.064 0.18 0 1 1 0 0.047 0.50 0 1 1 1 0.041 0.21 1 0 0 0 0.140 0.85 1 0 0 1 0.058 0.50 1 0 1 0 0.064 0.82 1 0 1 1 0.032 0.43 1 1 0 0 0.087 0.90 1 1 0 1 0.032 0.57 1 1 1 0 0.041 0.79 1 1 1 1 ---- ---- 76% 56% 43% 24% Cue Strength
Amnesia • Amnesics are not impaired for 1st 50 trials. Knowlton, Gluck & Squire, 1994
Huntington’s disease • Damage to the striatum • Impaired on probabilistic classification • A possible human correlate of habit learning. Knowlton et al. 1996
Methods • • • Baseline Predict Predict Baseline Predict Alternated blocks of prediction and baseline trials. 4 scans total 24 prediction trials per scan Participants: 8 right-handed, fluent English speakers Poldrack, R. A., Prabhakaran, V., Seger, C. A., & Gabrieli, J. D. E. (1999). Striatal activation during cognitive skill learning. Neuropsychology, 13, 564-574.
Probabilistic Classification Task: Classification > Baseline
Basal ganglia and hippocampus Right caudate (head) R medial temporal
Competition between MTL and striatal learning systems Probabilistic classification task (yellow, triangles) Paired associates task (blue, circles) Poldrack et al. 2001
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
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
Trial procedure While stimulus is on the screen, participants press key for rain or sun Correct 0 ms 2500 ms … 3000 ms 3500 ms
Stimulus - outcome relationships Stimulus Relationship P ( rain) 1 Deterministic 100 2 Deterministic 0 3 Probabilistic 90 4 Probabilistic 10 5 Probabilistic 80 6 Probabilistic 20 7 Random 50 8 Random 50 Baseline NA
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
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
Learning across blocks % correct 1 2 3 Block
Successful classification versus Baseline (Det-CP > base) and (Prob-CP > base) Right body / tail caudate % signal change 1 2 3 Block Left body / tail caudate 1 2 3 Block Z = 19
Areas associated with feedback: Head of the caudate Z = 19 Prob-CN > Prob-IN Ran-P > Ran-N
Interrelationships between hippocampal and caudate activity Det-CP Hippocampus Right caudate .47 # Left caudate .63 * Prob-CP Right caudate .00 Left caudate .04 Ran-P: Right caudate .33 Left caudate -.10 #: p < .1; *: p < .05 Ran-P > Ran-N
Correlations between blood flow and successful learning Right caudate-B1 Left caudate-B1 Accuracy .61 * .57 * Right hippocampus Accuracy-B1 -.59 * *: p < .05
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.
Category B Category A Category B Baseline Category A Baseline Stimulus set 1 (length-angle) Set 2: Length-width Ashby, Maddox, & Bohil (2002)
B 500 ms 250 ms XXXXX 2500 ms 250 ms 500 ms 250 ms Observational Learning
F 500 ms 250 ms Correct 2500 ms 250 ms 500 ms 250 ms Feedback Learning • Training portion
T 500 ms 250 ms XXXXX 2500 ms 250 ms 500 ms 250 ms Test trials: Observe and Feedback
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.
Classification performance on test trials Percentage Correct
Common classification activity: body and tail of caudate. Obs > Base Feed C > base
Feed C > base Head of caudate Percent Signal change Obs Obs- Base- Feed Feed- Base- test Obs test Feed
Hippocampus / MTL Obs > Base Feed C > Base
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