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The Journal of Neuroscience, 2001, 21:RC177:1-5
RAPID COMMUNICATION
Oscillatory Synchrony between Human Extrastriate Areas during
Visual Short-Term Memory Maintenance
Catherine
Tallon-Baudry1,
Olivier
Bertrand1, and
Catherine
Fischer2
1 Institut National de la Santé et de la
Recherche Médicale U280, 69003 Lyon, France, and
2 Neurological Hospital, 69003 Lyon, France
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ABSTRACT |
How do we keep an object in mind? Based on evidence from animal
electrophysiology and human brain-imaging techniques, it is commonly
held that short-term memory relies on sustained activity in a network
distributed over sensory and prefrontal cortices. How does neural
firing persist in such a distributed network in the absence of visual
input? Hebb's influential but so far unproved proposal, developed more
than 50 years ago, is that sustained activation in short-term memory
networks is maintained by reverberating activity in neuronal loops. We
hypothesized that synchronized oscillatory activity, proposed to
provide a dynamic link between distributed areas, could not only
coordinate activity in the network but also establish reentrant loops
in the system to enable both sustained firing and temporal coincidence
of inputs. We show in human intracranial recordings that limited
regions of extrastriate visual areas, separated by several centimeters,
become synchronized in an oscillatory mode during the rehearsal of an
object in visual short-term memory. Synchrony occurs specifically in
the  range (15-25 Hz) and disappears in a control condition. These
findings thus confirm experimentally the hypothesis of a functional
role of synchronized oscillatory activity in the coordination of
distributed neural activity in humans, and support Hebb's popular but
unproved concept of short-term memory maintenance by reentrant activity within the activated network.
Key words:
visual short-term memory; delayed-matching-to-sample
task; oscillations; synchrony; cell assembly; intracranial human
EEG
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INTRODUCTION |
Visual
short-term memory is thought to rely on the coordinated activity of
largely distributed networks involved in both the sensory processing
and storage of visual information (Goldman-Rakic, 1995 ; Fuster, 1997;
Magnussen, 2000). Sustained neural firing was observed in the
inferotemporal and prefrontal cortices of behaving monkeys during the
retention of information in visual short-term memory (Fuster and
Jervey, 1981; Miller et al., 1993; Wilson et al., 1993). Functional
magnetic resonance imaging in humans showed that short-term memory
maintenance is associated with activation of distributed regions in
visual extrastriate areas and in the prefrontal cortex (for review, see
Haxby et al., 2000). How is persistent firing maintained in the widely
distributed short-term memory network? It has been proposed that
oscillatory synchronization between spatially segregated cortical areas
could provide a flexible link between the different components of a network (Singer and Gray, 1995). Such recurrent synchronous patterns are consistent with the reentrant loops postulated by Hebb (1949) to
account for sustained neural activity during memory rehearsal. In
Hebb's model, sustained coincident firing is necessary to enhance synaptic efficiency, a key feature enabling the transition between short- and long-term memory. Oscillatory synchrony could underlie two
necessary features of Hebb's model, namely spike temporal coincidence
to modify synaptic efficiency and reverberating activity to maintain a
sustained firing. Although the effect of synchronous convergence of
inputs on synaptic plasticity is well documented in vitro or
in anesthetized animals (for review, see Paulsen and Sejnowski, 2000),
the existence of reentrant patterns of activity during memory
maintenance has not been demonstrated so far.
We intracranially recorded local neural activity in two epileptic
patients who had been stereotactically implanted with multicontact depth electrodes to monitor intractable epileptic seizures;
recording occurred while the patients performed a
delayed-matching-to-sample task (Fig. 1).
In both patients, we observed a sustained synchronized oscillatory
activity in the range (15-25 Hz) during the rehearsal of the
stimulus in short-term memory, between extrastriate visual areas
separated by several centimeters.
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Figure 1.
Block-designed paradigm. For the memory condition,
subjects had to press a button when the second shape was strictly
identical to the first one. Stimuli were randomly generated abstract
shapes presented during 400 msec, designed to minimize verbal
strategies and to foster visual imagery during the delay. For the
control condition, the button press was required when the brightness of
the fixation cross remained the same until the end of the delay. The
difficulty of both tasks was modulated on-line to keep the subject's
performance between 80 and 90% correct.
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MATERIALS AND METHODS |
Patients. Both patients (M.B., a 48-year-old female;
B.C., a 20-year-old female) suffered from pharmacologically resistant partial epilepsy and were candidates for surgery. Because the location
of the epileptic focus could not be identified using noninvasive
methods, they were stereotactically implanted with multicontact depth
probes. Contacts were 2 mm long and spaced every 3.5 mm
(center-to-center). Electrode locations were measured on x-ray images
obtained in a stereotactic frame and registered on structural magnetic
resonance images (MRIs). The accuracy of the registration procedure was
2 mm, estimated on another patient's MRIs obtained just after
electrode explantation and in which electrode tracks were still
visible. Both patients gave their informed consent to participate in
the experiment. Their visual fields and acuities were normal. The
signals described here were recorded away from the seizure focus (right
amygdalo-hippocampus complex in patient M.B., dysplasic lesion below
the right posterior calcarine sulcus in patient B.C.).
Paradigm. The experiment was divided into two conditions, a
memory condition and control condition, and was run in separate blocks
(Fig. 1). For the memory condition, subjects had to press a button when
the second stimulus exactly matched the first one. For the control
condition, they answered when the luminance of the fixation cross
remained the same until the end of the trial. The intertrial interval
was randomized between 2 and 3 sec. A new shape was randomly generated
at each trial. For both conditions, the difficulty of the task was
monitored on-line to keep the subject's performance between 80 and
90% correct. The details of stimulus construction and task difficulty
monitoring have been described previously (Tallon-Baudry et al., 1998,
1999). Both patients performed the tasks as normal subjects did
(Tallon-Baudry et al., 1999), at similar difficulty levels (coefficient
of shape deformation between S1 and S2; M.B., 12.0; B.C., 12.9; normal
subjects in the same paradigm; mean, 11.8; range, 10.5-12.6), and with
comparable performances (M.B., 84% correct; B.C., 83% correct; normal
subjects, 82.8% correct; range, 82.2-85.4%).
Recording and data analysis. A 64-channel continuous
depth-EEG was sampled at 1000 Hz (0.1-200 Hz bandwidth). The
electro-oculogram was monitored by surface electrodes. The
video-display refresh rate was 60 Hz (patient M.B.) or 100 Hz (patient
B.C.). To obtain a sufficient number of trials for statistical
analysis, data from the three delay periods (until 1200, 1600, and 2000 msec) were pooled and analyzed up to 1200 msec for each condition. The
analysis was restricted to the electrodes located in the visual
extrastriate cortex but outside of the epileptic focus (two depth
probes of 10 or 15 contacts each in each patient). Because the location of the implanted electrodes depended solely on clinical requirements, the prefrontal cortex was not investigated in these patients. Raw data
were visually inspected and any trial showing even small epileptic
spikes was discarded, leaving 125 and 116 trials for each condition,
respectively, for patient M.B. and patient B.C. There were not enough
error trials to analyze them. For each single trial, bipolar
derivations computed between adjacent electrode contacts were analyzed
in the time-frequency domain by convolution with complex Gaussian
Morlet's wavelets with a ratio f/ f of 14; the
frequency ranged from 8 to 80 Hz in 1 Hz steps (Tallon-Baudry and
Bertrand, 1999). At each time t and frequency f,
the result of the convolution for trial j is a complex
number
 where A represents the amplitude of the signal and  represents its phase. Synchrony between derivations k and
l is computed in the time-frequency domain across
n single trials as follows:
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This synchrony factor varies between 0 (independent signals) and
1 (constant phase-lag between the two signals). It should be noted that
the sign of the phase-lag measured here depends on the polarity of the
signal, which in the case of bipolar derivations is arbitrary. No
reliable conclusion can thus be drawn regarding the leading site. To
check whether a given value of the synchrony factor could be obtained
by chance, the significance of the existence of synchrony was assessed
in the time-frequency domain by randomization tests (Lachaux et al.,
1999) on shuffled data (5000 randomizations at each latency and
frequency). This statistical method detects only episodes of
synchronization that are not phase-locked to stimulus onset or offset
(i.e., that appear with a jitter in latency from one trial to the
next). To take into account the large number of samples tested, the
significance level of 0.05 was corrected by the number of frequencies
tested (72) and thus set at p  0.0006.
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RESULTS |
Recording sites
The areas investigated were all located anterior to V3A (DeYoe et
al., 1996; Tootell et al., 1997). In patient M.B., the most dorsal and
posterior focus was in the lateral occipital sulcus and could belong to
the object-responsive region located between areas V3A and MT (Tootell
et al., 1996). In patient B.C., the dorsal site was located in the
posterior parieto-occipital sulcus, a region found to be activated
during an object memory task requiring a high degree of spatial
precision (Faillenot et al., 1997). The more anterior and ventral sites
were located in the fusiform gyrus (patient M.B.) and in the inferior
temporal gyrus (patient B.C.). These regions have been shown to be
activated during visual object perception (Gauthier et al., 1999; Ishai
et al., 1999), imagery (Ishai et al., 2000), and short-term memory
(Postle and D'Esposito, 1999). The Talairach coordinates (in
millimeters) of the recording sites showing synchrony were (+27
 78 +12) and (+36 52 9) in patient M.B. and (+18 65 +18) and
(+61 53 5) in patient B.C.
Synchrony in the range during memory retention
Local signals were considered by computing the bipolar derivation
between two adjacent electrode contacts, separated by 3.5 mm. The
existence of a significant synchrony between two bipolar derivations
was computed in the time-frequency domain. In both patients, a
sustained significant synchrony in the range (15-25 Hz) could be
observed during the delay period for the memory condition. This
synchrony almost completely disappeared for the control condition (Figs. 2B,
3B). During the last 300 msec
of the delay (900-1200 msec), the mean synchrony factor in patient
M.B. at 20 Hz (B.C. at 16 Hz, respectively) was 0.331 for the memory
condition and 0.179 for the control condition (resp. 0.327 and 0.201).
At the end of the delay, the synchrony factor was thus increased by
>60% in both subjects for the memory condition compared with the
control and reached the significance level of 0.0006 for the memory
condition only. This phenomenon was restricted to a narrow frequency
range (17-24 Hz in patient M.B. and 15-17 Hz in patient B.C.) and
could readily be observed in some single trials (Figs.
2D, 3D).
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Figure 2.
Patient M.B. A, Electrode location
on coronal MRIs and projection on a lateral view of the brain in
Talairach coordinates. R, Right; L, left;
LOS, lateral occipital sulcus; Fus,
fusiform gyrus. The bipolar derivations considered at each site are
shown in red (LOS) and
blue (Fus) on the MRIs. B,
Time-frequency representations of the significance of synchrony between
the two sites for the memory (left) and control
(right) conditions. Time is presented on the
x-axis; frequency is shown on the y-axis
on a logarithmic scale. The delay period shared by all trials is
indicated in gray. Synchrony around 20 Hz ( range)
develops during memory rehearsal (red arrows). The
distribution of the between-site phase-lag at 20 Hz during the last 300 msec of the delay is presented on the rightmost panel.
C, Time course of the 20 Hz power of local oscillations
at both sites. The reference level (100%) is taken before stimulus
onset. Synchrony becomes significant at the 1% level at 468 msec and
at the 1 level at 500 msec, a latency at which the local signal
power has barely begun to rise. D, Example of a single
trial (top and middle rows, raw data,
0.1-200 Hz; bottom row, superimposed 15-25 Hz filtered
data). Synchronized oscillations were preceded by higher frequency
oscillations in the  range (30-100 Hz) that were most prominent in
the LOS.
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Figure 3.
Patient B.C. A, Electrode location
on coronal MRIs and projection on a lateral view of the brain in
Talairach coordinates. R, Right; L, left;
POS, parieto-occipital sulcus; ITG,
inferotemporal gyrus. The bipolar derivations considered at each site
are indicated in red (POS) and
blue (ITG). B,
Time-frequency representations of the significance of synchrony between
the two sites for the memory (left) and control
(right) conditions. Synchrony develops around 16 Hz
during the delay in the memory condition (red arrows).
The distribution of the between-site phase-lag at 16 Hz during the last
300 msec of the delay is shown in the rightmost panel.
C, Time course of the 16 Hz power of local oscillations
at both sites, for both conditions. D, Example of a
single trial (top and middle rows, raw
data, 0.1-200 Hz; bottom row, superimposed 12-20 Hz
filtered data).
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Despite the large distance between recording sites (3.5 cm in patient
M.B., 5.0 cm in patient B.C.), the mean time-lag observed in both
subjects was rather short: 5.4 msec in patient M.B. and 12.4 msec in
patient B.C. for oscillatory signals having a period of 50 and 62.5 msec, respectively. This lag was quite constant during the entire
rehearsal period, with 80% of the time samples during the last 300 msec of the delay showing lags of between 10 and 20 msec at 20 Hz in
patient M.B. and between 9 and 29 msec at 16 Hz in patient B.C.
(Figs. 2B, 3B, rightmost
panels).
An increase in between-area synchrony was not necessarily accompanied
by a power increase of the local oscillations at both sites. In patient
M.B., synchrony became significant for the memory condition at
p < 0.0006 at 506 msec. At this latency, the power of
local oscillations at both sites was smaller for the memory condition
than for the control condition (Fig. 2C). In patient B.C.,
the power of oscillations at the ventral site remained smaller for
the memory condition than for the control condition during the entire
delay period (Fig. 3C). The amount of between-site synchrony
thus seems to be independent of the amplitude of the signal at both sites.
Synchrony in other frequency bands
Although no sustained synchrony could be observed in the range
during the delay, local oscillations were present during stimulus
presentation, although not phase-locked to stimulus onset, at
frequencies that were markedly different across areas (52 Hz in the
lateral occipital sulcus and 74 Hz in the fusiform gyrus in patient
M.B., 60 Hz in the parieto-occipital sulcus and 38 Hz in the
inferotemporal gyrus in patient B.C.). Depending on the recording site,
oscillations either abruptly replaced activity at stimulus
offset or increased while activity slowly decreased.
Some sustained synchrony also occurred in the  range (10-12 Hz) in
patient M.B. (Fig. 2B), but it did not vary between
conditions. In the  range (3-6 Hz) in patient B.C., synchrony at 5 Hz became significant at the very end of the delay for the memory
condition. However, synchrony lasted only 130 msec for a signal at
5 Hz having a period of 200 msec, and thus cannot be considered as oscillatory. In addition, synchrony in the range does not
systematically accompany synchrony because synchrony was
completely absent in patient M.B. Sustained synchrony during memory
rehearsal thus seems specific to the 15-25 Hz band, at least between
the extrastriate areas investigated here.
Spatial selectivity of synchrony
The observed synchrony occurred between limited regions of cortex.
It decreased when neighboring pairs of electrodes were considered that
were a few millimeters away. Figure 4
shows the attenuation of the amount and significance of synchrony with
lateral distance. Coupling the dorsal site with a ventral site located 14 mm away from the ventral site showing the maximum synchrony led to a
decrease in the synchrony factor of >50% in both patients. Moreover,
synchrony during the delay remained significant for the neighboring
derivations (7 mm away) but not further laterally in both patients. The
long-distance synchrony spanning several centimeters illustrated in
Figures 2 and 3 thus cannot be attributable to a common source located
in between the dorsal and ventral sites and influencing both bipolar
derivations by simple volume conduction effects. Instead, this
synchrony occurs between small and well-delineated foci, extending over
a few millimeters of cortex but separated by several centimeters.
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Figure 4.
Spatial distribution of synchrony. The thickness
of the lines connecting bipolar derivations is proportional to the
amount of synchrony during the last 300 msec of the delay in the 17-24
Hz band (A, patient M.B.) and in the 15-17 Hz band
(B, patient B.C.). Synchrony between the pair of
derivations illustrated in Figures 2 and 3 is shown in
black, other pairs in gray. The
significance of synchrony during the delay is indicated by
asterisks (*p 0.01, **p 0.0006). synchrony remains significant
for the neighboring pair of electrodes but not further laterally.
R, Right; L, left; LOS,
lateral occipital sulcus; Fus, fusiform gyrus;
POS, parieto-occipital sulcus; ITG,
inferotemporal gyrus.
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DISCUSSION |
In both patients, synchronized oscillatory activity in the range between extrastriate visual areas occurred during rehearsal in
memory and thus could underlie the persistent and coordinated neural
activity in the short-term memory network in the absence of sensory
inputs. Synchrony was present during the entire rehearsal period in
patient M.B. but developed more gradually in patient B.C. Because the
difficulty of both tasks was modulated on-line to keep the subject's
performance between 80 and 90% correct, it seems unlikely that synchrony could reflect only an increased alertness level for the
memory condition compared with the control condition. In addition, synchrony developed during the delay period only, although subjects
were already highly attentive at stimulus onset. However, attentional
filtering and short-term memory are strongly intermingled processes
(for review, see Desimone and Duncan, 1995; Kastner and Ungerleider,
2000); for instance, to search for a face in a crowd (attentional
filtering), one has to activate and maintain a description of this face
(short-term memory).
Both patients were chronically treated with carbamazepine, an
anticonvulsant that decreases high-frequency sustained firing through
inactivation of voltage-dependent Na+
channels (Loscher, 1998). The day before and on the day of the recordings, patient M.B. had to receive in addition a benzodiazepine (chlobazam) that potentiates GABAA inhibition.
Both treatments may have modified the dynamics of the cellular network
involved in the generation of high-frequency oscillations (Gray and
McCormick, 1996; Traub et al., 1999) but are unlikely to produce focal
and task-dependent increases in synchrony. In addition, we observed similar variations of oscillations at the scalp level (right occipital electrode) in the same paradigm in normal unmedicated subjects (Tallon-Baudry et al., 1998).
We did not find any reliable evidence for memory-related synchrony
below 15 Hz or in the range (30-100 Hz). Thus our results do not
support directly the idea of an involvement of coupled /
synchrony in working memory processes (Lisman and Idiart, 1995;
Buzsaki, 1996; Sarnthein et al., 1998; Raghavachari et al., 2001) in
the extrastriate regions explored here. Moreover, synchronization in
the range is thought to involve the hippocampus, a structure that
may not be recruited in our task, which involved only a brief retention
interval, no spatial orienting, and no simultaneous memorization of
several distinct items. Rather than a co-occurrence of and oscillations, we observed a transition from local oscillations to a
between-area synchrony in the range. Oscillations followed by
between-site synchrony have also been observed in a completely
different preparation (in vitro in rat hippocampal slices)
after high-intensity tetanic stimulation. The tetanic stimulation
induces long-lasting changes in the occurrence and synchronization of
the oscillations, suggesting that they may be related to memory
processes (Whittington et al., 1997). The local oscillations in the range that we observed here could reflect the sensory processing
specific to each functional area, whereas the transition to a
synchronized distributed network at lower frequencies would enable the
rehearsal of the global neural representation of the stimulus. If
synchronous inputs in the range modulated the network synaptic
efficiency, it may in turn promote the long-term storage of this representation.
Our results point toward a role of sustained synchronized oscillatory
activity between extrastriate areas in the maintenance of an object
representation in human visual short-term memory. This extends previous
findings of high-frequency between-area synchrony observed in animal
recordings (Bressler et al., 1993; Roelfsema et al., 1997; vonStein et
al., 2000) and in human scalp EEG (Miltner et al., 1999; Rodriguez et
al., 1999) concerning primarily visuomotor integration, and thus
confirms experimentally the hypothesis of a role of oscillatory
synchrony in the coordination of neural activity in distributed
networks. Moreover, these findings may constitute the most direct
evidence obtained in vivo for reverberating activity through
reentrant circuits, which was postulated by Hebb (1949) a half a
century ago to account for sustained activation in short-term memory networks.
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FOOTNOTES |
Received June 15, 2001; revised July 18, 2001; accepted July 19, 2001.
We thank Jean Bullier and David Woods for their comments on an earlier
version of this manuscript.
Correspondence should be addressed to Catherine Tallon-Baudry, Institut
National de la Santé et de la Recherche Médicale U280, 151 cours Albert Thomas, 69003 Lyon, France. E-mail:
tallon-baudry{at}lyon151.inserm.fr.
This article is published in
The Journal of Neuroscience, Rapid Communications Section,
which publishes brief, peer-reviewed papers online, not in print. Rapid
Communications are posted online approximately one month earlier than
they would appear if printed. They are listed in the Table of Contents
of the next open issue of JNeurosci. Cite this article as:
JNeurosci, 2001, 21:RC177 (1-5). The
publication date is the date of posting online at
www.jneurosci.org.
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INTRODUCTION
