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

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 N WE Packard & McGaugh, 1996

Did injections of lidocaine to temporarily deactivate area.

Caudate Nucleus / Basal Ganglia Basal ganglia: Caudate Putamen Globus Pallidus Caudate and Putamen together are known as the striatum

SMA/PMC SSC Motor GP / SN thalamus DLPFC Parietal Spatial or Cognitive GP / SN thalamus Visual GP / SN thalamus Affective GP / SN thalamus Putamen Head of caudate Tail of caudate Ventral Striatum /NA VLPFC Inf temp Sup temp OFC, cing hipp, amg 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 l View set of cards l Decide if the cards indicate “rain” or “shine”

Category Structure CuesP(pattern)P(rain) %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 BaselinePredict Baseline Alternated blocks of prediction and baseline trials. 4 scans total 24 prediction trials per scan Participants: 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,

Weather Prediction: Behavior

Probabilistic Classification Task: Classification > Baseline

Basal ganglia and hippocampus Right caudate (head) R medial temporal

Competition between MTL and striatal learning systems Poldrack et al Probabilistic classification task (yellow, triangles) Paired associates task (blue, circles)

Outstanding questions  Reason for recruitment of striatum l Actual engram location? l Executive functioning? Feedback Uncertainty / Probabilistic nature of task l 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 Correct 0 ms 2500 ms … 3500 ms 3000 ms While stimulus is on the screen, participants press key for rain or sun

Stimulus - outcome relationships StimulusRelationship P ( rain) 1Deterministic100 2Deterministic0 3Probabilistic90 4Probabilistic10 5 Probabilistic80 6Probabilistic20 7Random50 8Random50 BaselineNA

 Participants: 15 young adults  Conditions analyzed l Stimulus type Det, Prob, Ran l Correctness C and I l Feedback received P and N l Examples Det-CP Det-IN Ran-P Ran-N Prob-CP Prob-IN Prob-CN Baseline

Comparisons  Areas associated with classification: l Conjunction analysis l Det-CP > baseline and Prob-CP > baseline  Areas associated with processing feedback: l Ran-P Ran-N l Prob-CP Prob-CN

Learning across blocks Block % correct

Right body / tail caudate Block Block % signal change Left body / tail caudate Successful classification versus Baseline (Det-CP > base) and (Prob-CP > base) 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 Ran-P > Ran-N 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

Right caudate-B1Left caudate-B1 Accuracy.61 *.57 * Correlations between blood flow and successful learning Right hippocampus Accuracy-B * *: p <.05

Study 2: Observational and Feedback learning  Basal ganglia play important role in learning via feedback l Feedback leads to better learning than observe in normal subjects on complex categorization tasks. l Learning via feedback is impaired in PD l Could be due to the DA reward circuits in the basal ganglia.

Stimulus set 1 (length-angle) Category A Category B Baseline Ashby, Maddox, & Bohil (2002) Category A Category B Baseline Set 2: Length-width

Observational Learning B 500 ms 250 ms2500 ms XXXXX 500 ms250 ms

Feedback Learning F 500 ms 250 ms2500 ms Correct 500 ms250 ms  Training portion

Test trials: Observe and Feedback T 500 ms 250 ms2500 ms XXXXX 500 ms250 ms

Methods  12 participants  Within subjects design: Each participant did both observe and feedback, counterbalanced, with different stimulus set.  Block design l Alternated task blocks with baseline blocks l 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

Head of caudate Obs Obs- Base- Feed Feed- Base- test Obs test Feed Percent Signal change Feed C > base

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 l Tail-body: stimulus-outcome mapping. Consistent with the “visual” corticostriatal loop l Head: related to processing feedback, expectancy, executive functioning. Consistent with the “cognitive” corticostriatal loop  Hippocampal - striatal antagonism not straightforward