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Nbetween them (e.g. [15–17,18

,19,20]), appear to con-
tribute to memory-relevant coding of information ranging
from objects (e.g. [21

]) to environmental locations (e.g.
[1

]). In addition, theta and gamma oscillations may help
to coordinate the interactions between regions required
by some mnemonic processing (e.g. [18

,22–24]) while
high frequency ‘ripples’ in the hippocampus may con-
tribute to consolidation (e.g. [25–28]). Furthermore, by
hippocampal formation is modulated in the theta band.
However, the firing of hippocampal place cells shows a
systematic phase relationship to the LFP theta rhythm.
Individual place cells fire whenever the animal enters a
specific part of its environment, so that together the place
cells encode the location of the animal relative to its
environment. However, the firing of place cells is modu-
lated at a slightly higher frequency than the LFP theta
www.sciencedirect.com Current Opinion in Neurobiology 2010, 20:143–149Brain oscillations and memory
Emrah Du¨zel
1,4,5
, Will D Penny
2
and
Oscillatory fluctuations of local field potentials (LFPs) in the
theta (4–8 Hz) and gamma (25–140 Hz) band are held to play a
mechanistic role in various aspects of memory including the
representation and off-line maintenance of events and
sequences of events, the assessment of novelty, the induction
of plasticity during encoding, as well as the consolidation and
the retrieval of stored memories. Recent findings indicate that
theta and gamma related mechanisms identified in rodent
studies have significant parallels in the neurophysiology of
human and non-human primate memory. This correspondence
between species opens new perspectives for a mechanistic
investigation of human memory function.
Addresses
1
UCL Institute of Cognitive Neuroscience, University College London,
WC1N 3AR London, United Kingdom
2
Wellcome Trust Centre for Neuroimaging, University College London,
WC1N 3BG London, United Kingdom
3
UCL Institute of Neurology, University College London, WC1N 3BG
London, United Kingdom
4
Institute of Cognitive Neurology and Dementia Research, Otto von
Guericke University, 39120 Magdeburg, Germany
5
German Centre for Neurodegenerative Diseases – Magdeburg, Otto
von Guericke University, 39120 Magdeburg, Germany
Corresponding author: Du¨zel, Emrah (e.duzel@ucl.ac.uk)
Current Opinion in Neurobiology 2010, 20:143–149
This review comes from a themed issue on
Cognitive neuroscience
Edited by Earl Miller and Liz Phelps
Available online 22nd February 2010
0959-4388/$ – see front matter
# 2010 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.conb.2010.01.004
Oscillations in the theta and gamma range can be
measured at different anatomical scales, ranging from
invasive recordings of small neuronal populations in
animals (e.g. [1

,2]) and humans (e.g. [3–5]) to non-
invasive recordings of large cortical assemblies from
the surface of the scalp using electroencephalography
(EEG) and magnetoencephalography (MEG) (e.g. [6–
14]). Both types of oscillation, and the phase relationshipseil Burgess
1,3
regulating the precise timing of presynaptic and postsyn-
aptic neurons, theta and gamma oscillations also modulate
spike-time dependent plasticity [29], a prerequisite for
both short-term and long-term memory processes.
Rhythmic activity in the rodent hippocampal
formation underlying spatial representation,
memory and consolidation
The systems neurophysiology underlying brain oscil-
lations and their relationship to memory has been exten-
sively studied using chronically implanted electrodes in
freely moving rodents. In this research there has been a
focus on the hippocampal formation, because of its central
role in memory, and also a focus on spatial representation,
because of the interesting spatial correlates of neural
firing found in and around the hippocampus, such as
the ‘place cells’ (e.g. [28]).
The theta rhythm and spatial representation
In freely moving rodents, the hippocampal LFP is domi-
nated by the theta rhythm whenever the animal is in
translational motion. This motion-related theta rhythm
increases in frequency with both age and running speed,
falling into a range from around 5 Hz to around 11 Hz.
During motion, power is also seen sporadically in the
gamma frequency band, with high (60–140 Hz) and low
(25–50 Hz) frequency gamma being associated with
different phases of theta [18

]. During immobility the
LFP shows ‘large irregular activity’ characterized by the
appearance of high frequency (200 Hz) ‘ripples’ or ‘sharp
waves’ (See [15,28] for reviews). Interestingly, there are
signs that human spatial navigation in virtual environ-
ments is also accompanied by the presence of theta
rhythmicity in intracranial recordings (e.g. [3]) and
MEG [12].
The hippocampal theta rhythm depends on a circuit
including the medial septum, hippocampus and entorh-
inal cortex and the projections between them. Lesions to
the medial septum both abolish movement related theta
and impair spatial memory while generators of theta are
also present in the hippocampus and entorhinal cortex
(see [15,28] for reviews). Consistent with the dominant
role of theta, the firing of the majority of neurons in the

144 Cognitive neurosciencefrequency so that their firing phase shifts from late to early
phases as the animal moves through the firing field [1

].
This ‘theta phase precession’ provides a phase code for
location, independent of the firing rate code which also
codes for location, but can be modulated by other factors
such as the objects, odors or actions occurring at the
location of the firing field [2].
Theta phase precession has also been observed in the firing
of ‘grid cells’ in the medial entorhinal cortex [30] – one of
the main neocortical inputs to the hippocampus. It is
possible that the regular spatial firing pattern of grid cells
[31] results from interference between theta band mem-
brane potential oscillations [32,33], and that the increase in
theta frequency with running speed relates to the temporal
firing pattern of these cells [34]. Interestingly, there is
evidence that similar spatial representations exist in human
entorhinal cortex, and that they contribute to spatial mem-
ory performance in virtual environments [35].
Oscillatory coordination of processing in multiple
regions
As well as providing a phase code for location within the
hippocampal formation, hippocampal theta also appears
to coordinate activity in other regions during the per-
formance of spatial tasks by rats. Thus, during spatial
memory tasks, theta activity coherent with that in hippo-
campus is seen in prefrontal cortex [23,36,37] and in
ventral striatum [38].
The high and low frequency gamma in CA1 that occurs at
specific phases of theta may coordinate flows of information
within the hippocampal formation [18

]: high frequency
gamma in CA1 is synchronized with high frequency
gamma in entorhinal cortex while low frequency gamma
in CA1 is synchronized with low frequency gamma in CA3.
Thus the inputs to CA1 from memory-related recurrent
processing in CA3 may occur at one phase of theta and be
characterized by low frequency gamma coherence, while
sensory-related input from entorhinal cortex may occur at a
different phase of theta and be characterized by high
frequency gamma. This would be consistent with the idea
that CA1 acts as a novelty detector by comparing mne-
monic and perceptual information (e.g. [19,39]), and with
the idea that encoding and retrieval occur at different
phases of the theta rhythm [40]. It also supports the idea
that theta and gamma oscillations in the hippocampal
formation work together to support memory [20]. Inter-
estingly, there is evidence from intracranial recordings in
humans, that phase coherence between rhinal (i.e. entorh-
inal and perirhinal) and hippocampal cortices in both
gamma and theta bands is predictive of subsequent mem-
ory performance [4,41], see below.Oscillatory coordination of reactivation/consolidation
It has long been thought that episodic information might
be rapidly stored within the recurrent connections of
Current Opinion in Neurobiology 2010, 20:143–149hippocampal region CA3 and then incorporated into
neocortical stores of long-term semantic memory [42].
One specific proposed mechanism is that the information
encoded during motion-related theta is transmitted to
neocortex by the coherent spiking of large populations of
hippocampal neurons during the sharp waves/ripples
occurring during subsequent immobility and slow wave
sleep, reviewed in [43]. Much subsequent research has
been consistent with this hypothesis: the activation pat-
terns of populations of place cells seen during awake
movement through an environment appear to be reiter-
ated on a faster timescale during the ripples/sharp wave
complexes of slow wave sleep (e.g. [25,26]). During
periods of awake immobility, it is possible to observe
both forward ‘preplay’ of the place cell representation of
upcoming locations and backward replay of recently
visited locations during ripple/sharp wave complexes
(e.g. [27,44]). Recent experiments have shown that se-
lective disruption of sharp wave/ripple complexes follow-
ing training in a spatial memory task impairs learning in
rats (e.g. [45]). In addition, there is evidence from intra-
cranial recording in humans that ripple-like oscillations at
80–140 Hz occur in both hippocampal and rhinal cortices,
and that the number recorded during resting (but not
necessarily sleeping) after encoding lists of pictures cor-
relates with subsequent memory for the pictures [46].
Brain oscillations and memory maintenance
Active short-term maintenance
Active short-term maintenance allows information from
transient events to persist in the brain as active repres-
entations. This enables goal-directed decision making and
learning to utilize and manipulate information beyond its
transient sensory availability. Slow oscillations in the delta
(1–3 Hz) and theta as well as faster oscillations in the beta
(12–25 Hz) and gamma ranges have been associated with
two major contributions during maintenance; coordinating
distributed cortical representations [14] and representing
encoded stimuli and their sequence of occurrence [21].
Theta networks of maintenance
Patients with bilateral hippocampal lesions are impaired in
their ability to maintain associative forms of information
even over short delays of a few seconds, while performing
normally for non-associative information. After a brief
presentation of a scene, for example, these patients are
unable to keep in mind the configural/relational association
of multiple features in the scene even for very short periods
of just a few seconds (e.g. [14,47]). A recent MEG study
showed that theta-synchrony between occipital and
temporal brain regions accompanied maintenance of con-
figural/relational (CR) information about photographs
depicting natural indoor or outdoor scenes, and was absent
in patients with bilateral hippocampal sclerosis [14]. Occi-pito-temporal theta-synchrony may indicate the coordina-
tion of cortical representations along the visual ventral
stream processing hierarchy, integrating anterior repres-
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