RESEARCH ARTICLE SUMMARY
◥
NEUROSCIENCE
Hippocampal sharp-wave ripples
linked to visual episodic recollection
in humans
Yitzhak Norman, Erin M. Yeagle, Simon Khuvis, Michal Harel,
Ashesh D. Mehta, Rafael Malach*
INTRODUCTION:Sharp-wave ripples (SWRs)
are rapid bursts of synchronized neuronal ac-
tivity elicited by the hippocampus. Extensive
study of SWRs, mainly in the rodent brain, has
linked these bursts to navigation, memory for-
mation, and offline memory consolidation. How-
ever, fundamental questions remain regarding
the functional meaning of this striking exam-
ple of network synchrony. Perhaps the most
glaring unknown is the relationship between
SWRs and conscious cognition. We still do
not know what cognitive process, if any, is
linked to the emergence of SWRs; to put it
simply, we still do not know what an animal
thinks about (if anything) when the hip-
pocampus elicits a ripple. Furthermore, the
potential role of SWRs in human episodic
memory is still largely unknown. Thus, study-
ing this phenomenon in conscious, awake
human patients opens a unique window, as
it allows direct examination of detailed verbal
reports with respect to SWR occurrences.
RATIONALE:We took advantage of the unique
ability of humans to communicate verbally
about their inner cognitive state to exam-
ine the role of SWRs in
memory formation and
retrieval, using intracranial
electrophysiological re-
cordings in patients. This
approach allowed us to
study free recall, the pro-
cess of self-initiated, inter-
nal generation of memories. It is a uniquely
powerful approach because it isolates the
process of recall from external stimulation.
RESULTS:Our study revealed three major
aspects linking SWRs to human declarative
memory. First, the SWR rate during picture
viewing (i.e., memory encoding) predicted
subjects’subsequent free-recall performance.
Second, a transient increase in SWR rate pre-
ceded the verbal report of recall by 1 to 2 s.
This increase was content-selective, recapitu-
lating the same picture preferences observed
during viewing. Finally, during recollection,
high-order visual areas showed content-selective
reactivation coupled to SWR emission.
CONCLUSION:By direct recordings of electro-
physiological events in the brains of individuals
who could inform, in real time, on their cogni-
tive state, we were able to demonstrate and
characterize an important role of SWRs in
human episodic memory. Our findings point
to the involvement of hippocampal SWRs in
establishing and triggering spontaneous re-
collections in the human brain. They implicate
SWRs in the process of engraving new memo-
ries, and reveal their fundamental contribution
in orchestrating the dialogue between memory
centers (hippocampus) and high-level repre-
sentations (cerebral cortex), which underlies
the retrieval of these memories. Our study thus
highlights the function of SWRs as powerful
multitasking signals that contribute both to
the encoding and to the spontaneous access
and reinstatement of human memories.▪
RESEARCH
Normanet al.,Science 365 , 657 (2019) 16 August 2019 1of1
The list of author affiliations is available in the full article online.
*Corresponding author. Email: [email protected]
Cite this article as Y. Normanet al.,Science 365 , eaax1030
(2019). DOI: 10.1126/science.aax1030
SWR-coupled re-activation of visual cortex during recall:
Category-selective
visual electrodes (n = 57 bipoles)
D
dB
-0.4
0
0.4
dB
-0.4
0
0.4
Time from picture onset (ms) Time from SWR onset (ms)
0
0.3
0 1000 2000 −400 0 400
dB
-4
0
4
0
2
4 PreferredNon-preferred
dB
-4
0
4
100
200
100
200
Free recall
non-preferred
preferred
Frequency (Hz)
preferred images
non-preferred images
100
200
100
200
Picture viewing
Cortical activation HFB power (dB)
B Free recall
1500 ms
750 ms
1500 ms
Picture viewing
CHippocampal Sharp Wave Ripples (SWR) re-activation during recall:
Left Hippocampus
A
P
0.2 mV
100 ms
10 μV
SWR
Picture viewing Free recall
Time from verbal recall onset (ms)
0.3
0.6
Time from picture onset (ms)
0
0.5
1
SWR rate (events/sec) 0 1000 2000 -4000 04000
High-RR images Low-RR images
CA1 electrode
Raw LFP
SWR
Ripple band
A
Hippocampal
electrodes
Cortical
electrodes
Intra-cranial recordings
Memory reactivation coupled to hippocampal ripples during free recall.(A) Simultaneous
intracranial recordings in hippocampus and cortex. (B) Patients first viewed and then freely
recalled photographs of famous faces and places. (C) Rapid hippocampal neuronal bursts
(SWRs) were identified (left). When patients freely recalled the images, a transient increase in
SWR rate anticipated the onset of recall, dominated by items that generated a higher ripple
rate (RR) during viewing (compare red and black lines). (D) Visual areas in the cortex showed
SWR-coupled reactivation, recapitulating the content selectivity observed during viewing.
ON OUR WEBSITE
◥
Read the full article
at http://dx.doi.
org/10.1126/
science.aax1030
..................................................