1. Neurobiology of Learning and Memory
Prof. Stephan Anagnostaras
Lecture 6: Multiple Memory Systems: Implicit Memory

2. Medial temporal lobe; diencephalon Classical conditioning
Different types of learning & memory rely on different brain structures
Explicit memory
Implicit memory
Medial temporal lobe; diencephalon
Priming
(neocortex)
Classical conditioning
Events
(episodic)
Procedural memory:
skills & habits
(basal ganglia)
Facts
(semantic)
Emotional Responses
(amygdala)
Skeletal musculature
(cerebellum)
Eyeblink conditioning in rabbit

3. Squire’s Taxonomy of Memory
Implicit memory is a broader term than explicit memory
Squire & Zola, PNAS, 1996

4. Basal Ganglia • Can examine Parkinson’s & early Huntington’s Disease
• no apparent amnesia (declarative memory ok)
But implicit memory problems in “procedural memory”
• Perceptual-Motor Learning
• Habits
• Skills
Separate from motor disorders

5. Serial Reaction Time (SRT) Task
Subjects are not told about the sequence.

6. SRT Results

7. Several perceptual motor tasks impaired by basal ganglia damage
• Serial Reaction Time
• Backwards Reading
• Prism adaptation
• Mirror drawing
• Also more cognitive tasks…

8. Knowlton, Mangels, & Squire, Science, 1996

9. Artificial Grammar Learning

10. Prototype Abstraction

11. Basal ganglia • Implicit learning deficits in several tasks
• Don’t need a motor component
• Can be quite “cognitive”
• No explicit memory necessary
• What about animals?

12. Packard, Hirsch & White, J Neurosci 1989 McDonald & White, Beh Neurosci 1993
% correct
Time spent

13. Win-Stay Acquisition Trials

14. Double dissociation paper: Electrolytic lesions on win-stay
Packard, Hirsh & White, J Neurosci, 1989

15. Win-Shift Training
Training Phase
Delay
Testing Phase
Baited

16. Double dissociation paper: Electrolytic Lesions on win-shift
Packard, Hirsh & White, J Neurosci, 1989

17. Triple D Histology (HPC + DLC)
McDonald & White, Behav Neurosci, 1993

18. Triple D: Neurotoxic DLC lesions impair win-stay learning
McDonald & White, Behav Neurosci, 1993

19. Triple D: Neurotoxic DLC lesions spare win-shift learning
McDonald & White, Behav Neurosci, 1993

20. Triple D: Neurotoxic HPC lesions impair win-shift learning
McDonald & White, Behav Neurosci, 1993

21. Triple D: Neurotoxic BLA lesions impair conditioned cue preference
McDonald & White, Behav Neurosci, 1993

22. Proposed characteristics of habit learning
Squire, 1992:
• Knowledge expressed through performance, rather than recollection
• Associations acquired across many trials
• Less flexible (less transferable) than declarative learning
Salmon & Butters, 1995:
“Habit learning refers to the formation of simple associations in
which a neutral stimulus comes to elicit a certain motor response
as a function of repeated reinforcement.”
Mishkin et al., 1984:
Product of processing is “not cognitive information, but a
non-cognitive simulus-response (S-R) bond…what is stored is not
objects, emotions…but the changing probability that a given stimulus
will evoke a specific response due to the reinforcement
contingencies at that time”

23. Sage & Knowlton, Beh Neurosci, 2000 US Devaluation of Win-Stay
(Testing the hypotheses)
Protocol:
Train
US devaluation
Test
• If performance does not involve representation of US, the CR should
remain intact (e.g., accurate, fast) on test. This would be consistent
with an S-R view.
• If performance mediated by representation of US, then recall of
devalued US should change the CR (e.g., inaccurate, slow) on test

24. Devaluation following win-stay acquisition

25. Win-stay late timepoint post-CTA trialsxx

26. Post-CTA win-stay accuracy summary
2, 9, or 22 days

27. Post-CTA win-stay latency summary* *
* = significant difference

29. Contextual Cuing Task (Chun & Phelps, Nat Neurosci, 1999)
Easy Version
Difficult Version

30. Contextual Cuing Task (Chun & Phelps, Nat Neurosci,1999)
Amnesics
2 anoxic
(1 conf hipp)
2 encephalitic
(2 conf hipp)
Implicit Learning Deficit in Amnesia !

31. Memory systems in Implicit Memory
• Not all implicit memory is independent of the hippocampus
• Not all implicit memory depends on the basal ganglia, e.g., emotional learning, priming, certain motor responses
• Cortical systems (e.g., priming)
• Amygdala (fear conditioning)
• Cerebellum (eyeblink conditioning)
…etc