Uncovering camouflage: amygdala activation predicts long-term memory of induced perceptual insight

Abstract

What brain mechanisms underlie learning of new knowledge from single events? We studied encoding in long-term memory of a unique type of one-shot experience, induced perceptual insight. While undergoing an fMRI brain scan, participants viewed degraded images of real-world pictures where the underlying objects were hard to recognize ("camouflage"), followed by brief exposures to the original images ("solution"), which led to induced insight ("Aha!"). A week later, the participants' memory was tested; a solution image was classified as "remembered" if detailed perceptual knowledge was elicited from the camouflage image alone. During encoding, subsequently remembered images were associated with higher activity in midlevel visual cortex and medial frontal cortex, but most pronouncedly, in the amygdala, whose activity could be used to predict which solutions will remain in long-term memory. Our findings extend the known roles of amygdala in memory to include promotion of long-term memory of the sudden reorganization of internal representations.

Figure 1

Example of a degraded real-world picture, or ‘camouflage’ image, used in the study. (For the original, ‘solution’ image see Figure 2 overleaf.)

Figure 2

The original picture, or ‘solution’ image used to generate Figure 1.

Figure 3

The protocol of Experiment 2. A. ‘study’ session, performed in the fMRI scanner. The session included 30 trials. Each consisted of: CAM1, the first camouflage exposure (participants press ‘YES’ if they think they identified the hidden object); ISI (inter stimulus interval, blank screen); SOL, solution (camouflage and original images alternate at 0.5 sec epochs); ISI; CAM2, a second camouflage exposure; QUERY, participants report their recognition at CAM1. Trials lasted 20-30 secs each and were separated by an intertrial intervals (ITI) of 3-6 secs. B. ‘test’ session, performed 7 days after the ‘study’, outside the scanner. This session included 40 trials: the 30 camouflage images presented in the ‘study’ session, interleaved with 10 novel images. In each trial, participants were given up to 10 secs to press a button if they recognized the camouflage image. They were then given a Multiple Choice recognition test (four alternatives), followed by a confidence rating (three levels). If they answered the Multiple Choice correctly, participants were presented with the camouflage image superimposed with a grid of numerals (Grid task), and instructions to find the numeral at the location of a specific feature in the image.

Figure 4

Forgetting curves in Experiment 1. Top panel, performance on the Multiple Choice task by separate groups of participants tested 15 minutes, 1 day, 7 days and 21 days after a ‘study’ session, respectively. Bottom panel, performance of the same groups on the subsequent Grid task. In both panels, images which participants recognized spontaneously during ‘study’ were excluded from the calculation of the percentages correct. The dashed lines depict average performance of all the groups on the 10 images not presented during ‘study’; these novel images were a different, randomly selected subset for each observer. For the slightly different ‘study’ protocol of Experiment 1 see Supplemental Figure S1.

Figure 5

During presentation of the solution images (SOL), the left amygdala was the brain region showing the greatest difference in activity between subsequently remembered and not remembered images (REM vs. NotREM). A. Sagittal and axial views of brain regions obtained by contrasting activation during SOL, collapsed across all trial types, with the baseline condition (blank screen). This analysis, which is unbiased with respect to subsequent memory or spontaneous recognition performance, was used to delineate the amygdala ROI. Other regions showing SOL-related activity are also shown (LO, lateral occipital; VOT, ventral occipito-temporal; dlPFC, dorso-lateral prefrontal cortex; lOFC, lateral orbital frontal cortex. For the full list see Supplemental Table S1.) B. Time-courses of activity during presentation of the camouflage image and its solution in the left amygdala. Left panel: percent-signal-change average during CAM1, sorted according to recognition performance as reported in the ‘study’ QUERY stage. Green, activity while observing spontaneously identified images (SPONT); purple, Not identified images (REM and NotREM collapsed). Right panel: percent-signal-change average during SOL. sorted according to subsequent memory performance in ‘study’. red, subsequently remembered (REM); blue, not remembered (NotREM). (The green curve again denotes activity while observing spontaneously identified images, SPONT).

Figure 6

Spontaneous identification and subsequent memory effects in mid-level visual cortex. Left panels: event-triggered average activity during CAM1, sorted according to recognition performance as reported in the ‘study’ QUERY stage. Green, activity while observing spontaneously identified images (SPONT); Purple, Not identified images. Right panels: averaged activity during SOL, sorted according to subsequent memory performance in ‘study’. red, subsequently remembered (REM); blue, not remembered (NotREM); green, spontaneously identified images (SPONT). The ROIs were delineated based on the visual localizer runs (see Experimental Procedures). LOC, lateral occipital complex; pFs, posterior fusiform sulcus. Time-courses presented here were extracted from the right hemisphere ROIs. For a view of these ROIs see Supplemental Figure S2.

Figure 7

Brain regions showing higher activity during presentation of the solutions of subsequently remembered camouflage images. Top Panels: A whole-brain analysis revealed a network of regions including foci in the left medial prefrontal cortex (mPFC); right anterior cingulate cortex (ACC); and the precuneus. (Medial views of left and right hemispheres; for the full list of significant foci see Supplemental Table S2.) Bottom panels: Percent-signal-change averages according to subsequent memory and independent recognition performance during SOL. Green, activation while observing the solution of spontaneously identified images (SPONT); red, subsequently remembered (REM); blue, not remembered (NotREM).

Figure 8

Memory prediction accuracy. Hit rate (y-scale; i.e. the number of trials in which the image was predicted to be remembered and was indeed recognized at the Grid task one week later, as a fraction of the total number of REM trials) and false-alarm rate (x-scale; i.e. the number of trials in which the image was predicted to be remembered, yet was not recognized at the Grid task one week later, as a fraction of the total number of NotREM trials) relation per subject. Each [blue/black] circle represents a participant. The dotted line depicts chance-level accuracy. For the ‘study’ protocol of Experiment 3, which was slightly different from that of Experiment 2, a view of the slice prescription used, and the time-courses of the amygdala ROIs see Supplemental Figure S3.