Priming, Implicit Memory, and the Brain: A Neuroimaging Perspective Daniel L. Schacter

1. Priming, Implicit Memory, and the Brain: A Neuroimaging Perspective Daniel L. Schacter Harvard University

2. Acknowledgements Memory Lab, Harvard Psychology Donna Addis Elissa Aminoff Elizabeth Chua Rachel Garoff-Eaton Angela Gutchess Dale Stevens Gagan Wig Alana Wong Athinoula A. Martinos Center for Biomedical Imaging Supported by NIMH and NIA

3. MYSTERY

4. APRICOT

5. CUPCAKE

6. ASSASSIN

7. _ _ES_ _X

8. _UP_ _KE

9. Tulving, Schacter, & Stark (1982)

13. Picture Fragment ID after 17 Years(M Age = 39.2; Mitchell, 2006)

14. Some Properties of Priming on Stem Completion, Fragment Completion and Identification Tests *Unaffected or even reduced by semantic or elaborative encoding manipulations that enhance recall and recognition. *Sensitive to changes between study and test in the physical features of target items: sensory modality, word font, case. Such changes typically have smaller effects on recall and recognition. *Typically preserved in amnesic patients with impairments on recall and reocgnition tests.

15. Characterizing Dissociations: Memory Systems Priming on tests such as completion and identification is little affected by semantic processing and highly dependent on physical features of stimuli. Led to postulation of perceptual representation system (‘PRS’): involves storage/retrieval of modality- specific information that supports identification of words/objects (Schacter, 1990;Tulving & Schacter, 1990). “Pre-semantic” collection of susbsystems (visual word form, auditory word form, structural description) that depend on posterior cortical brain regions, not hippocampus/MTL; should be preserved in amnesia.

16. + + + + + + + + + + + + 2 SEC BETWEEN STIMULI Object Priming Paradigm STUDY TEST

17. + + Behavioral Performance at Test 900 850 800 750 700 REACTION TIME (MSEC) 650 600 550 500 450 0 REPEATED NOVEL

18. Priming-related activation decreases Novel > Repeated Same Reduced activation (indicating priming) for repeated objects in multiple regions, including: • Left anterior inferior frontal cortex (BA 47, 45) • Bilateral fusiform, extending into parahippocampal cortex (BA 37, 19)

19. Specificity of Priming-Related Reductions Neural correlates of priming for: • Novel objects • Repeated same objects • Repeated different objects 18 subjects scanned while undertaking size judgements of visually-presented objects. Koutstaal et al. (2001) Neuropsychologia

20. Fusiform Laterality Effect Repeated Different > Repeated Same Greater activation (indicating less priming for Different) in: • Bilateral fusiform (BA 37, 19). • Greater effect of exemplar change in Right than Left fusiform cortex

22. Explaining Activation Decrease in Object Priming “Neural Tuning” Wiggs, C. L., & Martin, A. (1998). Properties and mechanisms of perceptual priming. Current Opinion in Neurobiology.

23. 1.Start Phase “Bigger than a shoebox? (yes/no)” Novel Novel Novel Low Prime Novel Low Prime High Prime High Prime 2.Switch Phase 3.Return Phase “Smaller than a shoebox? (yes/no)” “Bigger than a shoebox? (yes/no)” Novel Low Primed High Primed Low Primed Novel High Primed Is Object Priming Response Specific? n = 16, Event Related, 4 - Cycles Dobbins, Schnyer, Verfaellie & Schacter (2004) Nature

24. Is Object Priming Response Specific? a 1100 Start Switch Return 1000 900 Mean Reaction Time - milliseconds 800 700 600 Low Novel High Cue Reversal - fMRI Dobbins, Schnyer, Verfaellie & Schacter (2004) Nature

25. Mean “Neural Priming” -15 Start Switch Return 0.12 .30 .30 0.08 .20 .20 0.12 PFC .10 .10 Forgetting Control 0.04 0.10 .00 .00 0.08 0.00 PFC 0.06 0.04 Fusiform -0.04 0.02 0.00 -0.02 Fusiform Start Switch Return Is Object Priming Response Specific? Dobbins, Schnyer, Verfaellie & Schacter (2004) Nature

26. -15 Is Object Priming Response Specific? Relation to Behavior Both fusiform and PFC “neural priming” scores predicted behavioral priming scores, each accounting for unique variance. PFC (not fusiform) neural priming predicted size of behavioral slowing that occurred when cue was switched…suggests that lack of activity is a marker of automaticity.

27. Is there a correlation between behavioral & neural priming? Frontal Temporal Perceptual -Dobbins et al. (2004) -Maccotta & Buckner (2004) -Lustig & Buckner (2004) -Bergerbest et al. (2005) -Golby et al. (2005) -Oranfidou et al. (2006) -Bunzeck et al. (2006) -Turk-Browne et al. (2006) -Carlesimo et al. (2003) -Dobbins et al. (2004) -Turk-Browne et al. (2006)

28. Least Most Stimulus Specificity A multiple component model of priming A R L Schacter, Wig & Stevens (2007). Curr Opin Neurobiol

29. Least Most Stimulus Specificity A multiple component model of priming A D A R L -Amodal -Priming across abstract representations -Sensitive to changes in stimulus-decision mapping Schacter, Wig & Stevens (2007). Curr Opin Neurobiol

30. Least Most Stimulus Specificity A multiple component model of priming A D A R L -Amodal -Priming across abstract representations -Sensitive to changes in stimulus-decision mapping -Most consistently correlated with behavior Schacter, Wig & Stevens (2007). Curr Opin Neurobiol

31. Study Phase • For each of 3 runs at study, 144 shapes were presented (16 sets of 9 exemplars) • Each set alternated in spatial position to the right or left of fixation • Pres. Time = 2.5 sec Nonstudied Prototype Exemplar Exemplar • Instructions: remember each shape and side of the screen Slotnick Schacter (2004) Nature Neuroscience

32. Left fusiform gyrus (BA18) 0.3 0.2 0.1 Early visual regions (BA17, BA18) % Signal change 0 -0.1 -0.2 -0.3 0 8 4 12 16 Time (sec) Old-hits Related-false alarms True recognition > False recognition Ventral View LH Old-hits > Related-false alarms X Related-false alarms > Old-hits

33. Left fusiform gyrus (BA37) 0.2 0.1 % Signal change 0 -0.1 Late visual regions (BA19, BA37) -0.2 0 8 4 12 16 Time (sec) Left cuneus (BA18) Early visual regions (BA17, BA18) 0.4 0.2 % Signal change 0 -0.2 Old-hits Old-misses New-correct rejections 0 8 4 12 16 Time (sec) Nature of visual area activity? Ventral View *Old-hits > Old-misses should reflect conscious recollection *Old-hits + Old-misses expected to reflect nonconscious activity LH Old-hits > Old-misses Old-hits + Old-misses

34. Line Orientation Task *For each shape (at ‘study’ or ‘test’), speeded response whether internal lines sloped: 1) upward 2) downward *Subjects were not informed that any shapes would be repeated.

35. Left lingual gyrus (BA18) 0.2 * Early visual regions (BA17, BA18) 0.1 % Signal change 0 -0.1 0 8 4 12 16 Time (sec) Old Related Line Judgment Task: Old>Related Ventral View * No late visual region activity (BA19,BA37) LH Old > Related X Related > Old Slotnick & Schacter (2006) Neuropsychologia

36. Line Judgment Task: Behavioral Results * * 980 970 960 ns 950 Reaction Time (ms) 940 930 920 910 Old Related New * p < 0.05 Slotnick & Schacter (2006) Neuropsychologia

37. Least Most Stimulus Specificity A multiple component model of priming A D A R L -Amodal -Priming across abstract representations -Sensitive to changes in stimulus-decision mapping -Most consistently correlated with behavior Schacter, Wig & Stevens (2007). Curr Opin Neurobiol