Yadin Dudai & Kelly Ludmer Neurobiology Dept. Weizman Institute of Science

1. Uncovering Camouflage: The Neural Basis of Long-Term Memory for One-Shot Perceptual Exposure Nava Rubin Center for Neural Science New York University Yadin Dudai & Kelly Ludmer Neurobiology Dept. Weizman Institute of Science

2. Abrupt transitions in perceptual organization 4

3. Abrupt transitions in perceptual organization (Rubin, Nakayama and Shapley, 1997, 2004) 4

4. Hebb (1949): “is insight or hypothesis -- or, in the broadest terms, intelligence -- something distinct from the mechanism of association?” [In order to induce insight, one needs] “tasks ... of just the right degree of difficulty ... [they] must neither be so easy so that the animal solves the problem at once, thus not allowing to analyze the solution; nor so hard that the animal fails to solve it except by rote learning in a long series of trials.” 6

5. 1 - 0.5 - 0 - Fraction responses “thin” Inducers’ rotation (deg) Illusory Shape Discrimination Task “thin” or “fat”? (Ringach & Shapley, 1996) 8

6. 100 ms Abrupt improvement in performance 10

7. Trial-by-trial analysis of performance over time (10 observers) 12

8. Abrupt improvement in performance - specific to retinal size! 14

9. 8

10. Perceptual Learning: Prevailing Paradigms and Findings Incremental, Watanabe et al 2002 Stimulus-specific Ahissar And Hochstein 2000 common conclusion: (neurally) early learning site(s) 18

11. Hebb (1949): “insight ... continually affects the learning of the adult animal … it is not wholly separate from rote learning.” Hebb proposed a unitary mechanism, based on the associations of co-occurring internal states, within which to understand all learning phenomena. However, he emphasized that the sequence of internal states is not merely determined by external events, but is rather an active process in which the animal is continually attempting to discover structure and meaning in the incoming information. 20

12. Abrupt Perceptual Learning of Camouflage Images: demo 22

13. Making camouflage images: Original  Gaussian blur (1 free parameter: s) B/W threshold (2nd free param, q) However, not all images lend themselves to becoming good camouflages. Many images are “too easy” even after blur+thresholding: … whereas others are not “perceptually compelling” even after seeing the solution: (“two-tone”) 24

14. Camouflage images vary in how perceptually compelling the are. Also, observers vary in how compelling they judge a particular image to be. Conjecture: the degree to which a camouflage is perceptually compelling (after being shown the solution) will have an effect on how likely it is to be remembered in the future. 26

15. Ingredients of the camouflage paradigm Perceptual (re-)organization Bottom-up/top-down interactions Perceptual learning Spontaneous insight (“Aha!”) or Induced insight Encoding Consolidation Short- and long-term recognition ~Episodic memory  A rich yet relatively controlled paradigm to study perceptual learning, short- and long-term memory formation. } Perception (Previously studied, e.g. Dolan et al 1997) } Memory 28

16. Induced Insight Protocol: the ‘study’ phase (30 images per observer, out of a pool of 40 images total) If you think you identified the object, press “Yes” spontaneous recognition: 30% 30

17. Induced Insight Protocol: the ‘test’ phase Performed on 30 images from ‘study’ +10 novel images Administered to three different groups: 10 min, 1 day, 7 or 21 days after study Up to 10 sec Up to 10 sec Up to 10 sec 32

18. The memory curve (each time point a is from a different group of 10-12 observers) ‘study’ 34

19. Brain Imaging of Induced Insight • 17 subjects (3 eliminated; 9/14 men) • fMRI scanning during the ‘study’ phase • ‘Test’ phase a week later (outside the magnet). • 3T Siemens Allegra scanner • Quadra coil, 36 slices, 4mm, ac-pc • 3x3 mm voxels • TR=2 sec 36

20. …. “Rem “NotRem” “Rem” “Spont” .… Subsequent Memory Analysis ‘Study’ phase events are classified according to the behavioral performance during ‘Test’: (Note: ‘spont’ determined already at ‘study’ time) 38

21. …. …. “Rem “NotRem” “Rem” “Spont” .… Terminology, within-trial sub-events: CAM1 SOL CAM2 (10 sec) (4 sec) (2 sec) Terminology, trial type classification: 40

22. Analysis • Generate cortical “regions of interests” (ROIs) from contiguous voxels that showed higher activation during the SOL (all event types) than during blank control trials. • Compare the event-triggered average time-courses* of each ROI for the different event types (Rem, NotRem, Spont) * - or alternatively deconvolved time-courses 42

23. ROI Results: Visual Cortex SPONT NoRec Rem NoRem early vis cortex (V1/V2) % signal change 0 2 4 6 8 10 12 [sec] 0 2 4 6 8 10 12 [sec] LOC Mid-level visual areas predict subsequent SOL memory 0 2 4 6 8 10 12 [sec] 0 2 4 6 8 10 12 [sec] pFs (aka VOT) …and hi-level vis areas (VOT/pFs) do not! 0 2 4 6 8 10 12 [sec] 0 2 4 6 8 10 12 [sec] 44

24. ROI Results: Amygdala SPONT NoRec Rem NoRem % signal change 0 2 4 6 8 10 12 [sec] 0 2 4 6 8 10 12 [sec] Activity in the amygdala during SOL viewing is the strongest predictor for subsequent SOL memory 46

25. Results: whole brain GLM analysis (REM>NoRREM) 18

26. Conclusions The degree to which a camouflage image is perceptually compelling, as manifested by LOC activity, will have an effect on how likely it is to be remembered in the future. There is an involvement of an emotional component: camouflage images that survive in long term memory are associated with greater activity in the amygdala. 50