1. FMRI studies of the human basal ganglia learning system Carol A. Seger Cognitive and Behavioral Neuroscience programs Department of Psychology Colorado State University

2. p.314 W. W. Norton

3. Memory and Habit  Habit: Slowly acquired associations between stimuli and responses/outcomes.  Memory: Memory for particular episodes

4. 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

5. Did injections of lidocaine to temporarily deactivate area.

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

7. 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

8. Striatal learning in humans  Problem: Humans use the medial temporal lobe memory system for tasks that other animals learn using the striatal system.

9. Probabilistic Classification  Task l View set of cards l Decide if the cards indicate “rain” or “shine”

10. Category Structure CuesP(pattern)P(rain) 0000-------- 00010.1400.15 00100.0840.38 00110.0870.10 01000.0840.62 01010.0640.18 01100.0470.50 01110.0410.21 10000.1400.85 10010.0580.50 10100.0640.82 10110.0320.43 11000.0870.90 11010.0320.57 11100.0410.79 1111-------- 76%56%43%24% Cue Strength

11. Amnesia  Amnesics are not impaired for 1st 50 trials. Knowlton, Gluck & Squire, 1994

12. Huntington’s disease  Damage to the striatum  Impaired on probabilistic classification  A possible human correlate of habit learning. Knowlton et al. 1996

13. 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, 564- 574.

14. Weather Prediction: Behavior

15. Probabilistic Classification Task: Classification > Baseline

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

17. Competition between MTL and striatal learning systems Poldrack et al. 2001 Probabilistic classification task (yellow, triangles) Paired associates task (blue, circles)

18. 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

19. 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

20. Trial procedure Correct 0 ms 2500 ms … 3500 ms 3000 ms While stimulus is on the screen, participants press key for rain or sun

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

22.  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

23. 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

24. Learning across blocks 1 2 3 Block % correct

25. Right body / tail caudate 1 2 3 Block 1 2 3 Block % signal change Left body / tail caudate Successful classification versus Baseline (Det-CP > base) and (Prob-CP > base) Z = 19

26. Areas associated with feedback: Head of the caudate Z = 19 Prob-CN > Prob-IN Ran-P > Ran-N

27. 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

28. Right caudate-B1Left caudate-B1 Accuracy.61 *.57 * Correlations between blood flow and successful learning Right hippocampus Accuracy-B1 -.59 * *: p <.05

29. 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.

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

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

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

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

35. 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.

36. Classification performance on test trials Percentage Correct

37. Common classification activity: body and tail of caudate. Obs > Base Feed C > base

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

39. Hippocampus / MTL Obs > Base Feed C > Base

40. 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