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Workshop (Rep. No. 8, Arctic System Science, Seattle, 1998). D. G. Geophys. Res. Lett. 25, 17291732 (1998). are periodic and cover a broad frequency
9. Steele, M. & Boyd, T. J. Geophys. Res. 103, 1041910435 (1998). 12. Stockton, C. W. & Glueck, M. F. Longterm Variability of the North range (from less than 2 to greater than
10. Dickson, B., Meincke, J., Vassie, I., Jungclaus, J. & Osterhus, S. Atlantic Oscillation (NAO) (Annu. Mtg, Am. Met. Soc., 1999).
Nature 397, 243246 (1999). 13. Rahmstorf, S. & Ganopolski, A. Clim. Change (in the press).
60 Hz), indicating that neurons in the cere-
11. McPhee, M. G., Stanton, T. P., Morison, J. H. & Martinson, 14. Maslowski, W. et al. EOS Trans. 79, 414 (1998). bral cortex can oscillate synchronously in
various frequency bands.
Neurobiology The new studies1,2 concentrate on the so-
called gamma frequency range, which is cen-
Striving for coherence tred around 40 Hz. The authors selected this
frequency because precise synchronization
Wolf Singer
of neuronal responses is often associated
with oscillations in the 40-Hz range5. But
o explain how the brain interprets the predictions derived from this hypothesis. it is not trivial to detect these oscillations.

T world, Descartes postulated that we


have a single centre the pineal gland
where all sensory signals converge and
Signals from the EEG reflect, with high tem-
poral resolution, the activity of many neu-
rons in the cortical area beneath the elec-
Synchronized firing is usually short-lived
(100300 ms) and, except for an initial com-
ponent, the oscillations are not phase-locked
are evaluated jointly, where decisions are trodes. This prevents precise localization of to the stimulus because they are self-generat-
reached and future actions planned. But neuronal responses, but facilitates the detec- ed. This prevents averaging and requires a
progress in neurobiology has forced us to tion of synchronous activity. The responses method that allows brief bursts of synchro-
adopt a different view that nowhere do we of distributed neurons summate effectively nous activity to be detected in single trials.
have a single centre to evaluate or coordinate and then give rise to measurable fluctua- New analytical tools have made it possible
computations. So how are the results of tions of the EEG signal only if they are well to confirm that these transient gamma-
many parallel computations bound together synchronized. Typically, EEG fluctuations oscillations exist in the human brain, and
to permit coherent perception and action?

E. RODRIGUEZ
On pages 430 and 434 of this issue,
Rodriguez et al.1 and Miltner et al.2 address
this question by investigating the temporal
coherence of electroencephalographic
(EEG) signals recorded from people per-
forming cognitive tasks.
To represent perceptual objects or motor
programmes in systems that do not con-
verge, the idea is that a particular content is
represented by jointly activating an assembly
of cells, rather than by the response of an
individual, highly specialized neuron3. The
advantage is that an almost unlimited num-
ber of different assemblies each represent-
ing different contents can be generated,
because subsets of cells drawn from the large
(but limited) pool of functionally specialized
neurons in the cerebral cortex can be dynam-
ically regrouped. However, this mechanism
must allow the neurons that participate in a
particular assembly to be identified unam-
biguously. The responses of all the neurons
in a particular assembly must then be
labelled, to ensure that they are processed
jointly at subsequent stages.
Based on theoretical considerations4 and
data from multi-electrode recordings in the
visual cortex5, it has been proposed that
responses are bound together and labelled
by synchronized firing of the individual
neurons with a millisecond precision. The
assumption is that such synchronized activi-
ty summates more effectively than non-
synchronized activity in the target cells at
subsequent processing stages. If so, synchro-
nization could increase the effect that a
selected group of neurons has on other pop-
ulations with great temporal specificity.
Jointly raising the effect of a subset of
responses is equivalent to functional binding
because it favours further joint processing of Figure 1 Mooney faces used by Rodriguez et al.1. Mooney faces are easily recognizable when viewed
the selected responses. upright, but not when inverted. The authors used them to show that, in humans, neurons oscillating
The EEG studies by Rodriguez et al.1 and at a frequency of 40 Hz can synchronize across different regions of the brain. Miltner et al.2 asked
Miltner et al.2 were designed to test the subjects to associate visual and tactile stimuli, and found similar coherence of oscillations at 40 Hz.

NATURE | VOL 397 | 4 FEBRUARY 1999 | www.nature.com 1999 Macmillan Magazines Ltd 391
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to establish close relations between them the area representing the non-conditioned
and cognitive processes6,7. hand. Finally, the increased coherence was
Rodriguez et al. and Miltner et al. now confined to a narrow band around 40 Hz,
show that local oscillatory responses can supporting the idea that synchronization of
synchronize across different cortical areas oscillations in this frequency range is
the time course and topological distribu- involved in cognitive processes.
100 YEARS AGO tion of synchronization showed a high The new results provide further evidence
The vexed question as the exact meaning degree of task-related specificity. These that synchronization might allow the sel-
of the phrase one hour after sunset and results from humans closely resemble those ective association of distributed neurons.
one hour before sunrise in the Local obtained by intracortical recording from However, neither these nor previous studies
Government Act, 1888, referring to the cats8. Rodriguez et al.1 asked people to have demonstrated this in the vertebrate
lighting of bicycle lamps, was settled inspect pictures that could, on occasion, be brain, because we cannot yet disrupt syn-
from a legal point of view in a Divisional recognized as a face (Fig. 1). They found that chronization in the relevant frequency band
Court on Thursday last. It had been held scrutinizing the pictures was associated with without affecting other response variables.
that sunset at Greenwich was meant, and increased gamma activity over cortical But a functional role for synchronization has
the Bristol justices convicted a cyclist for regions known to be involved in visual pro- been demonstrated in the insect olfactory
riding a bicycle without a light an hour cessing. But precise phase-locking of these system9. There is also indirect evidence from
after sunset thus defined. The alleged oscillations across cortical areas occurred psychophysical studies, which suggests that
offence was committed on August 19, only when the subjects identified a face. This the brain binds responses together and inter-
1898, at 8.15 p.m., which was less than state of heightened synchrony was transient. prets them as related if they are made syn-
an hour after sunset at Bristol, but more It dissolved shortly before the subjects chronous by synchronizing the stimuli that
than an hour after sunset at Greenwich. responded by pressing a key, giving way to a evoke them1012. If the brain interprets
An appeal was made against the second episode of phase-locked gamma responses as related when they are made syn-
decision of the Bristol magistrates; and activity associated with the motor response, chronous by internal mechanisms (as was
at Thursdays Court the appeal was which had a different topological distribu- the case in the people studied by Rodriguez et
allowed, and the conviction quashed, tion. The authors suggest that such dynamic al.1 and Miltner et al.2), gamma oscillations
their Lordships holding that the phrase in changes in the phase relations between spa- could well be the mechanism that binds neu-
the Act referred to must not be tially distributed oscillating groups of neu- rons into functionally coherent assemblies.
understood to mean Greenwich time, but rons could reflect the transient formation of Wolf Singer is at the Max Planck Institute for Brain
local time. assemblies that are bound by synchrony and Research, Deutschordenstrasse 46, D-60528
From Nature 2 February 1899. represent first perception of the stimulus Frankfurt/Main, Germany.
and then the motor programme. e-mail: singer@mpih-frankfurt.mpg.de
50 YEARS AGO Miltner et al.2 tested the hypothesis that if 1. Rodriguez, E. et al. Nature 397, 430433 (1999).
The medical, social and economic people learn the association between a visual 2. Miltner, W. H. R., Braun, C., Arnold, M., Witte, H. & Taub, E.
Nature 397, 434436 (1999).
problems created by a rapidly ageing and a tactile stimulus, they should form a 3. Hebb, D. O. The Organization of Behavior (Wiley, New York,
population were the subject of a neuronal assembly comprising cells respon- 1949).
symposium at the British Association sive to the visual and the tactile stimuli, 4. von der Malsburg, C. Ber. Bunsenges. Phys. Chem. 89, 703710
meeting at Brighton on Friday, September respectively. The authors observed a marked (1985).
5. Gray, C. M., Knig, P., Engel, A. K. & Singer, W. Nature 338,
10, 1948. The subject was introduced by increase of gamma activity after the visual
334337 (1989).
Sir Ernest Rock Carling, who reminded stimulus was presented. Notably, they also 6. Tallon-Baudry, C., Bertrand, O., Delpuech, C. & Pernier, J.
his audience that the great majority of the found a selective increase of gamma coher- J. Neurosci. 17, 722734 (1997).
elderly are healthy and independent ence between the visual cortex and the corti- 7. Tallon-Baudry, C., Bertrand, O., Peronnet, F. & Pernier, J.
they outnumber the ailing and decrepit by cal area representing the hand that had J. Neurosci. 18, 42444254 (1998).
8. Roelfsema, P. R., Engel, A. K., Knig, P. & Singer, W. Nature
more than 30 to 1 and for them the received the tactile stimulus. This coherence 385, 157161 (1997).
most pressing problem is how to maintain must have developed as a consequence of 9. Stopfer, M., Bhagavan, S., Smith, B. H. & Laurent, G. Nature
to the end of their days the standard of conditioning, because it disappeared when 390, 7074 (1997).
living of their working life. The time has the learnt association was lost (that is, after a 10. Leonards, U., Singer, W. & Fahle, M. Vision Res. 36, 26892697
(1996).
come for the elderly to revolt against the sequence of visual stimuli not connected to a 11. Alais, D., Blake, R. & Lee, S.-H. Nature Neurosci. 1, 160164
convention, based on sociological, not tactile stimulus were presented). Moreover, (1998).
biological, grounds, that there is a fixed such coherence was not seen for signals from 12. Usher, M. & Donnelly, N. Nature 394, 179182 (1998).
retirement-age beyond which they are
unfit for further work. It is a truism that Mathematics
chronological age is no guide to capacity
in the individual; but what we want to Counting up to four
know is, how far the increased
Ivar Ekeland
expectation of life in the last fifty years
has extended working-capacity. Ageing
begins at birth, and an athlete is old at lace marbles in a straight line. You can nth being then at a distance 2n12d from the (n
thirty-five. ... Laziness, Sir Ernest
maintained, is at the bottom of much
facile acceptance of too old at forty, fifty,
P always arrange them so that they are
not evenly spaced. But can you
arrange them so that no subset of k marbles,
1 1)th. But then the distance between the
marbles grows extremely fast, and they are
spaced more and more widely apart: the den-
or sixty. If the Civil servant must retire, including non-neighbours, for k 3, is sity of the alignment (that is, the proportion
why does not the clergyman? If the evenly spaced (Fig. 1, overleaf)? Again, the of occupied sites between the first and the
barrister ceases to practice, why not the answer is yes: if d is the distance between the last one) tends to zero as the number of mar-
judge? first two marbles, just put the third one at bles increases. What happens if we impose
From Nature 5 February 1949. distance 2d from the second one, the fourth non-zero density? The answer is that for any
at distance 22d from the third, and so on, the integer k and non-zero density d there will be
NATURE | VOL 397 | 4 FEBRUARY 1999 | www.nature.com 1999 Macmillan Magazines Ltd 393

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