Hippocampal Sharp Wave Ripples Improve Memory
Science 14 Jun 2019:Vol. 364, Issue 6445, pp. 1082-1086DOI: 10.1126/science.aax0758
Long-duration hippocampal sharp wave ripples improve memory
Antonio Fernández-Ruiz, et.al.
New York University Neuroscience Institute, New York University, New York, NY 10016, USA.
Department of Neuroscience and Zuckerman Mind Brain Behavior Institute, Columbia University, New York, NY
10027, USA.
Center for Mathematics, Computing and Cognition, Universidade Federal do ABC, São Bernardo do Campo, São
Paulo, Brazil.
Division of Neurosciences, University Pablo de Olavide, 41013 Seville, Spain.
Center for Neural Science, New York University, New York, NY 10016, USA.
[paraphrase]
Hippocampal sharp wave ripples (SPW-Rs) have been hypothesized as a mechanism for
memory consolidation and action planning. The duration of ripples shows a skewed
distribution with a minority of long-duration events. We discovered that long-duration
ripples are increased in situations demanding memory in rats. Prolongation of
spontaneously occurring ripples by optogenetic stimulation, but not randomly induced
ripples, increased memory during maze learning. The neuronal content of randomly induced
ripples was similar to short-duration spontaneous ripples and contained little spatial
information. The spike content of the optogenetically prolonged ripples was biased by the
ongoing, naturally initiated neuronal sequences. Prolonged ripples recruited new neurons that
represented either arm of the maze. Long-duration hippocampal SPW-Rs replaying large
parts of planned routes are critical for memory.
Sharp wave ripples (SPW-Rs) in the hippocampus are considered a key mechanism for
memory consolidation and action planning. SPW-Rs are composed of the sharp wave, a
negative polarity deflection in the CA1 apical dendritic layer, which reflects the magnitude
of the CA3 excitatory input, and the ripple, a short-lived fast oscillatory pattern (140 to
200 Hz) of the local field potential (LFP) in the CA1 pyramidal layer. The duration of
ripples exhibited a skewed distribution. A minority of long-duration ripples was interspersed
among a majority of short- and intermediate-duration events. We hypothesized that long-
duration ripples are related to mnemonic demand and, therefore, examined ripple statistics
across a variety of tasks in rats.
Our findings demonstrate that a simple measure, such as the duration of SPW-Rs, can
provide valuable information about the underlying neuronal computations. Learning and
correct recall in spatial memory tasks were associated with extended SPW-Rs. Closed-
loop optogenetic prolongation of CA1 ripples improved working memory
performance, whereas aborting the late part of ripples decreased performance. Prolongation
of CA1 ripples did not induce repeated spiking of the already active neurons but instead
recruited spikes from the low-firing population of pyramidal cells and increased the
diversity of the participating neurons. Neurons recruited during the artificially elongated
portion of ripples had place fields preferentially in the side arms of the maze. This feature of
the optogenetically prolonged ripples resembled those in spontaneous long ripple events. In
contrast, randomly induced ripples recruited largely the same neurons as in short spontaneous
ripples. We hypothesize that the neuronal trajectory of optogenetically induced events
depends on the contemporaneous brain state, with SPW-Rs and inter-SPW-R periods
referring to different network states. Once a trajectory has been selected at the onset of a
SPW-R, artificial recruitment of additional neurons via optogenetic perturbation is
constrained by the attractor dynamic of the CA1 network. This observation supports the idea
that CA1 neuronal sequences are computed locally in CA1 rather than being fully inherited
from upstream regions. Alternatively, SPW-Rs are embedded in larger networks, including
entorhinal and neocortical areas, and the differential effects of closed-loop and random
stimulation might be determined by the network state in areas upstream from CA1. In
either case, diversification of neurons, covering large segments of planned routes, may
explain the memory-improving effect of both spontaneous long and closed loop–prolonged
ripples
[end of paraphrase]
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