NEUROSCIENCE:
Drums Keep Pounding a Rhythm in the Brain
Michael P. Stryker*
The rhythmic activity of neurons in the brain has
fascinated neuroscientists ever since electrical potentials were first
recorded from the human scalp more than 70 years ago. The rhythms of
electrical activity in sensory neurons that encode visual information
are known to vary markedly with attention. How does neuronal encoding
differ for a visual stimulus that is the center of attention compared
with one that is ignored? To answer this question, Fries et al. (1)
simultaneously recorded electrical activity from several clusters of
neurons in the V4 region of the visual cortex of macaque monkeys that
were shown behaviorally relevant and distracter objects (see the
figure). On page 1560
of this issue, they report a rapid increase in the synchronization of
electrical activity in the gamma frequency range (35 to 90 Hz) in V4
neurons activated by the attended stimulus (that is, the stimulus on
which attention is focused) but not in V4 neurons activated by
distracter objects (1).
The benefits of paying attention. A halo of attention
surrounds one of the two physically similar stimuli (vertical and
horizontal stripes) that the monkey can see while his eyes fixate on a
point between them. The attended stimulus has a more powerful
representation in the V4 area of the visual cortex because the neurons
that respond to it tend to fire rhythmically in synchrony with one
another, as illustrated by the wiggly trace to the right of the
stimulus. V4 neurons that respond to the other (distracter) stimulus
fire at similar rates but not in synchrony. Synchronized firing
provides the attended stimulus with a more powerful representation,
illustrated by the greater clarity of the mental image.
SOURCE FOR BRAIN: CARIN CAIN
The
neurophysiology of attention remains a puzzle. A simple and attractive
hypothesis is that an attended stimulus behaves as though it were
bigger and brighter than all of the other competing stimuli. To encode
this bigger and brighter stimulus, neurons would need to somehow
increase their electrical response. Although some experiments have
shown the production of a greater (but still equally selective)
neuronal electrical discharge in response to attention (2, 3), other studies in the same brain areas have found almost no effect of attention on electrical activity (4),
and in still others the effects of attention were disappointingly
small. So, it would be attractive indeed to discover a
neurophysiological mechanism for attention that is consistent with all
of these findings.
About 12 years ago, rhythmic oscillatory activity and neuronal
synchronization were proposed as solutions to a different but related
problem. In higher mammals, including monkeys and humans, there are
many different visual areas in the brain that respond more or less
selectively to the different qualities of a visual stimulus: its
motion, color, texture, and so on. When more than one object is
visible, how are the representations of the different qualities of the
individual objects bound to one another so that a person does not
associate the color of one object with the movement of another? The
Singer (5) and Eckhorn groups (6)
suggested that the widespread representations of the different visual
qualities of a particular object might be unified by neurons firing
together rhythmically on a time scale of 25 milliseconds or so, with
representations of different objects encoded in electrical activity of
different phases or frequencies. Crick and Koch (7)
suggested that the same sort of synchronous oscillation might underlie
consciousness or visual awareness. Extreme manipulations of visual
awareness--such as presenting a viewer's two eyes with different scenes
that alternately appear and disappear (a phenomenon called binocular
rivalry--have provided some support for this proposal. However, it has
not yet been demonstrated with more natural stimuli that the presence
of rhythmic or synchronous activity among a collection of neurons
controls whether the features represented by those neurons are bound
together either to represent a single object to our perceptual system
or to bring an object into conscious awareness. A stringent test of
this hypothesis would be to use ambiguous figures (such as the classic
face-vase illusion) in which the same physical stimulus can be
perceived in different ways, to determine whether the way the object is
perceived depends on which clusters of neurons are firing together (8).
In a sense, the Fries et al.
study brings us full circle. Their experiments show that it is the
rhythmic coordination of a subpopulation of neurons, and not just the
amount of nerve cell activity per se, that is associated with finding
what we are looking for and missing the unexpected. Their work suggests
that the rhythmic synchrony of electrical signals may not be the
hallmark of perceptual unity or of conscious awareness. Instead it may
be a consequence of a decision to focus attention on a relevant
stimulus. A synchronous neural response makes the representation of the
stimulus more prominent and thereby more likely to enter the
consciousness of the viewer.
The basic biophysical properties of neurons and synapses allow rhythmic
synchronization to enhance the effect of a fixed amount of neuronal
activity both in sensory neurons in the periphery and in the brain's
central processing stations, which receive inputs from these neurons.
The enhancing effect of synchronous activity would cause larger
responses to the attended stimulus in neurons at the next stage of
signal processing. At each stage of processing, responses to the
attended stimulus would become stronger, whereas those to the
distracter stimuli would remain weak or would fade away entirely.
Despite the attractiveness of this proposal, it is not at all clear how
attention causes responses to become more oscillatory and better
synchronized. Modifying the strength of particular cortical
interneuronal circuits could, in principle, favor certain frequencies
of electrical discharge, but it is not known whether or how such
circuits receive the inputs that turn them on.
Perhaps it makes sense to regard rhythmic synchronization as only one
of a number of processes that enhance responses to attended stimuli.
Other processes might include increases in background or "spontaneous"
discharges (9)
or changes in neuronal "gain." At least for these two hypotheses, there
are clear pharmacological demonstrations that different classes of
synaptic receptors can have additive or multiplicative effects on
neuronal activity (10).
It is also important to note that rhythmic synchronization may be
important in other activities besides attention to a stimulus. For
example, synchronization may be used to signal the persistence of
stimuli even when the neurons responding to those stimuli with
increased rates of discharge do so only transiently (11).
Finally, one must remember that synchronization has its costs as well
as its benefits. Pooling the outputs from many neurons adds information
only if the activity of those neurons is not coordinated. Zohary et al. (12)
have shown that the information provided by many thousands of neurons
in a higher cortical visual area is only marginally greater than that
provided by a few neurons in that area if the electrical discharges of
the many are simultaneous. Thus, even minimal synchronization can
drastically limit the ability of the cortex to take advantage of its
vast numbers of neurons.
References
- P. Fries, J. H. Reynolds, A. E. Rorie, R. Desimone, Science 291, 1560 (2001).
- J. H. Reynolds et al., Neuron 26, 703 (2000) [Medline].
- S. Treue, J. H. Maunsell, J. Neurosci. 19, 7591 (1999) [Medline].
- E. Seidemann, W. T. Newsome, J. Neurophysiol. 81, 1783 (1999) [Medline].
- C. M. Gray et al., Nature 338, 334, (1989) [Medline].
- R. Eckhorn et al., Biol. Cybern. 60, 121 (1988) [Medline].
- F. Crick, C. Koch, Cold Spring Harbor Symp. Quant. Biol. 55, 953 (1990) [Medline].
- M. P. Stryker, Nature, 338, 297 (1989) [Medline].
- G. Fernandez et al., Hippocampus 9, 35 (1998) [Medline].
- K. Fox, H. Sato, N. Daw, J. Neurophysiol. 64, 1413 (1990) [Medline].
- R. C. deCharms, M. M. Merzenich, Nature 381, 610 (1996) [Medline].
- E. Zohary et al., Nature 370, 140 (1994) [Medline].
The author is in the Keck Center for Integrative Neuroscience,
Department of Physiology, University of California, San Francisco, CA
94943-0444, USA. E-mail: stryker@phy.ucsf.edu
Related articles in Science:
- Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention
-
Pascal Fries, John H. Reynolds, Alan E. Rorie, and Robert Desimone
Science 2001 291: 1560-1563.
(in Reports)
[Abstract]
[Full Text]
Volume 291,
Number 5508,
Issue of 23 Feb 2001,
pp. 1506-1507.
Copyright © 2001 by The American Association for the Advancement of Science. All rights reserved.
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