Hippocampal sharp-wave ripples linked to visual episodic recollection
Science 16 Aug 2019: Vol. 365, Issue 6454, eaax1030
Hippocampal sharp-wave ripples linked to visual episodic recollection in humans
Yitzhak Norman, et.al.
Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel.
Department of Neurosurgery, Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, and Feinstein
Institute for Medical Research, Manhasset, NY 11030, USA.
[paraphrase]
Sharp-wave ripples (SWRs) are rapid bursts of synchronized neuronal activity elicited
by the hippocampus. Extensive study of SWRs, mainly in the rodent brain, has linked
these bursts to navigation, memory formation, and offline memory consolidation.
However, fundamental questions remain regarding the functional meaning of this striking
example 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 hippocampus elicits a ripple. Furthermore, the
potential role of SWRs in human episodic memory is still largely unknown. Thus, studying
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.
We took advantage of the unique ability of humans to communicate verbally about their
inner cognitive state to examine the role of SWRs in memory formation and retrieval,
using intracranial electrophysiological recordings in patients. This approach allowed us to
study free recall, the process of self-initiated, internal generation of memories. It is a
uniquely powerful approach because it isolates the process of recall from external
stimulation.
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
preceded the verbal report of recall by 1 to 2 s. This increase was content-selective,
recapitulating the same picture preferences observed during viewing. Finally, during
recollection, high-order visual areas showed content-selective reactivation coupled to SWR
emission.
By direct recordings of electrophysiological events in the brains of individuals who could
inform, in real time, on their cognitive 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
recollections in the human brain. They implicate SWRs in the process of engraving new
memories, and reveal their fundamental contribution in orchestrating the dialogue between
memory centers (hippocampus) and high-level representations (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.
Hippocampal sharp-wave ripples (SWRs) constitute one of the most synchronized
activation events in the brain and play a critical role in offline memory consolidation. Yet
their cognitive content and function during awake, conscious behavior remains unclear. We
directly examined this question using intracranial recordings in human patients engaged
in episodic free recall of previously viewed photographs. Our results reveal a content-
selective increase in hippocampal ripple rate emerging 1 to 2 seconds prior to recall
events. During recollection, high-order visual areas showed pronounced SWR-coupled
reemergence of activation patterns associated with recalled content. Finally, the SWR rate
during encoding predicted subsequent free-recall performance. These results point to a role
for hippocampal SWRs in triggering spontaneous recollections and orchestrating the
reinstatement of cortical representations during free episodic memory retrieval.