effect implicates the involvement of SWRs in
memory formation.
Our observation that SWRs tend to emerge
rather frequently during a visual memory task
that is clearly nonspatial in nature demonstrates
that SWRs are not exclusive to navigational as-
pects, but rather play a more general role in
episodic memory ( 14 ). This is compatible with
the occurrence of SWRs during a visual search
task in primates ( 18 ).
Finally, an important aspect of SWR function
uncovered by the current study is the content-
selective coupling between SWRs and cortical
activation. This content selectivity, reflected in
HFB activity in high-order cortical sites, was
precisely time-locked to the SWR event itself.
Thus, SWR-triggered activity in high-order visual
sites was significantly higher when patients re-
called items that preferentially activated these
sites during picture viewing. Reactivation of
visual content occurred most prominently during
the time window of the SWR. The SWR-triggered
cortical activity was specific to the actual recall
events and was not found during the search
times between verbal recalls. This result further
attests to the specific role of this activity in
reportable, conscious recollection.
Previous work in rodents ( 27 , 61 ) has dem-
onstrated a bidirectional interaction between
the hippocampus and the cortex during mem-
ory consolidation and retrieval. Such studies
suggested a role for the cortex in facilitating
reactivation of the relevant hippocampal repre-
sentation during a SWR. Consistent with these
suggestions, previous work in humans ( 43 )has
demonstrated a slow, anticipatory activation of
category-specific cortical information that pre-
cedes the actual moment of recall by severalseconds ( 44 , 62 ). Moreover, during internal mem-
ory search, when subjects attempt to recall a
particular category but fail to come up with a
specific exemplar, activity in category-specific
cortical sites remains slightly elevated, possibly
reflecting a top-down control signal that imposes
categorical boundaries on downstream memory
representations in the hippocampus ( 44 ). Our
findingofaslighttrendofanadvancedcortical
activation prior to SWR onset is compatible with
the suggested top-down cortical influence and
the bidirectional nature of the hippocampal-
cortical interplay in general, although further
research will be required to fully characterize
and confirm this interaction.
Our results are consistent with recent work by
Vaz and colleagues ( 63 ) showing coupled ripple-
band activity in MTL and temporal association
cortex during successful retrieval. Both spectralNormanet al.,Science 365 , eaax1030 (2019) 16 August 2019 9of14
Recall decoder
cross-classification performance
Exemplar identity (peak: 21.4%)Recall decoder
cross-classification performance
Category (peak: 82.1%)-400 -200 0 200 400
Time from ripple onset (ms)5060708090Decoding accuracy (%)p=0.05-400 -200 0 200 400
Time from ripple onset (ms)0102030Decoding accuracy (%)p=0.05A B
D E F
faces C
places2
PC2-2
0
-2PC10 -2
2PC3^02PCA
picture-viewing response
(83.8% explained variance)Item #(^11528) faces places
5
10
PC #
score
-3
0
3
-400 -200 0 200 400
0
500
1000
1500
2000
-0.3
0
0.3
corr. (r)
Time from ripple onset (ms)
RECALL
VIEWING
Time from picture onset (ms)
t 1 t 2 t 3 tn t 1 t 2 t 3 tm
sliding window
Free Recall
(ripple-triggered activity)
Picture viewing
Pearson correlation (r)
PC 1
PC 11
PC 2
time (50 ms bins)
sliding window
time (50 ms bins)
Fig. 6. Similarity between recall decoding performance and cortical
activation patterns during viewing and free recall.(A) PCA applied to
multivariate activation patterns during picture viewing. Note that the first
principal component (accounting for 40% of the variance) captured the
categorical difference between items. (B) Visualizing the patterns
according to PC1, PC2, and PC3 showed a clear categorical clustering of
faces and places, with some additional differentiation at the item level.
(C) After dimensionality reduction, Pearson correlation was used to
quantify the similarity between viewing and recall patterns, with a 50-ms
sliding window ( 91 ). (D) Viewing-recall pattern similarity relative to the
SWR event and to the onset/offset of the pictures (black horizontal
lines). Significant correlation was found only during the SWR event
(P< 0.05, cluster-based permutation test; significant clusters are
contoured in black). (EandF)Performanceofk-NN classifier trained on
viewing patterns and tested on recall patterns (cross-classification).
Shaded gray area shows the decoding performance for shuffled data
(mean ± SD). Dashed orange lines represent the cluster-defining
threshold (P= 0.05); significant time clusters are marked above
(P< 0.01, cluster-based permutation test). For visualization, decoding
performance was smoothed using a boxcar filter three time bins wide.
RESEARCH | RESEARCH ARTICLE