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The Meaning
ofDreams
By Jonathan Winson
Throughout history, human beings have sought to understand the meaning of dreams.
The ancient Egyptians believed dreams possessed oracular pow- state, a period of several minutes when thoughts consist of frag-
er— in the Bible, for example, Joseph’s elucidation of Pharaoh’s mented images or minidramas. The hypnogogic state is followed
dream averted seven years of famine. Other cultures have in- by slow-wave sleep, so called because at that time the brain
terpreted dreams as inspirational, curative or alternative reality. waves of the neocortex (the convoluted outer mantle of the
During the past century, scientists have offered conflicting psy- brain) are low in frequency and large in amplitude. These sig-
chological and neuroscientific explanations for dreams. In nals are measured as electroencephalographic (EEG) recordings.
1900, with the publication of The Interpretation of Dreams, Researchers also discovered that a night’s sleep is punctu-
Sigmund Freud proposed that dreams were the “royal road” to ated by periods in which the EEG readings are irregular in fre-
the unconscious, that they revealed in disguised form the deep- quency and low in amplitude— similar to those observed in
est elements of an individual’s inner life. awake individuals. These periods of mental activity are called
More recently, in contrast, dreams have been characterized REM sleep. Dreaming takes place solely during these periods.
as meaningless, the result of random nerve cell activity. Dream- While in REM sleep, motor neurons are inhibited, preventing
ing has also been viewed as the means by which the brain rids the body from moving freely but allowing extremities to remain
itself of unnecessary information— a process of “reverse learn- slightly active. Eyes move rapidly in unison under closed lids,
ing,” or unlearning. breathing becomes irregular, and heart rate increases.
Based on recent findings in my own and other neuroscien- The first REM stage of the night follows 90 minutes of slow-
tific laboratories, I propose that dreams are indeed meaningful. wave sleep and lasts for 10 minutes. The second and third REM
Studies of the hippocampus (a brain structure crucial to mem- periods follow shorter slow-wave sleep episodes but grow pro-
ory), of rapid eye movement (REM) sleep and of a brain wave gressively longer themselves. The fourth and final REM inter-
called theta rhythm suggest that dreaming reflects a pivotal as- val lasts 20 to 30 minutes and is followed by awakening. If a
pect of the processing of memory. In particular, studies of theta dream is remembered at all, it is most often the one that oc-
rhythm in subprimate animals have provided an evolutionary curred in this last phase of REM sleep.
clue to the meaning of dreams. They appear to be the nightly This sleep cycle— alternating slow-wave and REM sleep—
record of a basic mammalian memory process: the means by appears to be present in all placental and marsupial mammals.
which animals form strategies for survival and evaluate current Mammals exhibit the various REM-associated characteristics
experience in light of those strategies. The existence of this pro- observed in humans, including EEG readings similar to those
cess may explain the meaning of dreams in human beings. of the awake state. Animals also dream. By destroying neurons
in the brain stem that inhibit movement during sleep, research-
Stages of Sleep and Dreaming ers found that sleeping cats rose up and attacked or were star-
T H E P H Y S I O L O G Y O F D R E A M I N G was first understood in tled by invisible objects— ostensibly images from dreams.
1953, when researchers characterized the human sleep cycle. By studying nonprimate animals, scientists have discovered
They found that sleep in humans is initiated by the hypnogogic additional neurophysiological aspects of REM sleep. They de-
cord) and that during REM sleep neural signals—called pontine- determined sleep cycle. Yet the central concept of Freud’s theo-
geniculate-occipital (PGO) cortex spikes— proceed from the ry—namely, the belief that dreams reveal a censored representa-
brain stem to the center of visual processing, the visual cortex. tion of our innermost unconscious feelings and concerns— con-
Brain stem neurons also initiate a sinusoidal wave (one resem- tinues to be used in psychoanalysis.
bling a sine curve) in the hippocampus. This brain signal is called Some theorists abandoned Freud altogether following the
theta rhythm. neurological discoveries. In 1977 J. Allan Hobson and Robert
At least one animal experiences slow-wave but not REM McCarley of Harvard Medical School proposed the “activa-
sleep— and, consequently, does not exhibit theta rhythm when tion-synthesis” hypothesis. They suggested that dreaming con-
asleep. This animal is the echidna, or spiny anteater, an egg-lay- sists of associations and memories elicited from the forebrain
ing mammal (called a monotreme) that provides some insight (the neocortex and associated structures) in response to ran-
into the origin of dreaming. The absence of REM sleep in the dom signals from the brain stem such as PGO spikes. Dreams
echidna suggests that this stage of the sleep cycle evolved some were merely the “best fit” the forebrain could provide to this
140 million years ago, when marsupials and placentals diverged random bombardment from the brain stem. Although dreams
from the monotreme line. (Monotremes were the first mammals might at times appear to have psychological content, their
to develop from reptiles.) bizarreness was inherently meaningless.
By all evolutionary criteria, the perpetuation of a complex The sense, or plot, of dreams resulted from order that was
brain process such as REM sleep indicates that it serves an im- imposed on the chaos of neural signals, Hobson said. “That or-
portant function for the survival of mammalian species. Un- der is a function of our own personal view of the world, our re-
derstanding that function might reveal the meaning of dreams. mote memories,” he wrote. In other words, the individual’s
ANATOMY OF THE BRAIN and cross section of the hippocampus show some of the regions involved
in dreaming. In the hippocampus, incoming information is processed sequentially in the dentate
Vanderwolf of the University of Western
gyrus and the CA3 and the CA1 pyramidal cells (so named for their triangular shape). In nonprimate Ontario discovered there was one behav-
species, the theta rhythm brain wave is generated in the dentate gyrus and the CA1 cells. ior during which the animals he studied,
THETA RHYTHM
Exploration
Apprehension
Predation
THETA RHYTHM brain signal is present during different waking behaviors in vival. In placental and marsupial animals, theta rhythm is present during
different species. Each of these behaviors is pivotal to the animal’s sur- rapid eye movement (REM) sleep.
including the rat, showed theta rhythm: which theta rhythm was generated in the James B. Ranck, Jr., of the State Universi-
REM sleep. hippocampus. Together with the neocor- ty of New York Downstate Medical Cen-
In 1972 I published a commentary tex, the hippocampus is believed to pro- ter and his then co-worker Susan Mitchell
pointing out that the different occurrenc- vide the neural basis for memory storage. identified a third synchronous generator
es of theta rhythm could be understood The hippocampus (from the Greek word in the entorhinal cortex, and Robert
in terms of animal behavior. Awake ani- for “seahorse,” which it resembles in Verdes of Wayne State University dis-
mals seemed to show theta rhythm when shape) is a sequential structure composed covered the brain stem neurons that con-
they were behaving in ways most crucial of three types of neurons. Information trol theta rhythm. These neurons trans-
to their survival. In other words, theta from all sensory and associational areas mit signals to the septum (a forebrain
rhythm appeared when they exhibited of the neocortex converges in a region structure) that activate theta rhythm in
behavior that was not genetically encod- called the entorhinal cortex; from there it the hippocampus and the entorhinal cor-
ed— such as feeding or sexual behavior— is transmitted to the three successive neu- tex. Thus, the brain stem activates the
but rather a response to changing envi- ronal populations of the hippocampus. hippocampus and the neocortex— the
ronmental information. Predatory be- The signal arrives first at the granule cells core memory system of the brain.
havior in the cat, prey behavior in the of the dentate gyrus, then at the CA3 To determine the relation between
rabbit, and exploration in the rat are, re- pyramidal cells (so called because of their theta rhythm and memory, I made a le-
spectively, most important to their sur- triangular shape) and finally at the pyra- sion in the rat septum. Rats that had pre-
vival. For example, a hungry rat will ex- midal cells of CA1. After information is viously learned, using spatial cues, to lo-
plore before it eats even if food is placed processed by this trio of cells, it is re- cate a particular position in a maze were
in front of it. transmitted to the entorhinal cortex and no longer able to do so after their septums
then back to the neocortex. were disabled. Without theta rhythm,
Role of Theta Rhythm My studies showed that theta rhythm spatial memory was destroyed.
FURTHERMORE, because the hippo- was produced in two regions within the Studies of the cellular changes that
campus is involved in memory process- hippocampus: the dentate gyrus and the bring about memory illustrated the role
ing, the presence of theta rhythm during CA1 neurons. The rhythms in these two of theta rhythm. In particular, the dis-
REM sleep in that region of the brain areas were synchronous. Subsequently, covery in 1973 of long-term potentiation
might be related to that activity. I sug-
gested that the theta rhythm reflected a JONATHAN WINSON started his career as an aeronautical engineer, graduating with an en-
THE AUTHOR
neural process whereby information es- gineering degree from the California Institute of Technology in 1946. He completed his Ph.D.
sential to the survival of a species— gath- in mathematics at Columbia University and then turned to business for 15 years. Because
ered during the day— was reprocessed of his long-standing interest in neuroscience, Winson then began research at the Rocke-
PATRICIA J. WYNNE
into memory during REM sleep. feller University on memory processing. In 1979 he became associate professor there and
In 1974, by recording signals from continued his work as professor emeritus, retiring in 1996. His research was supported
the hippocampus of freely moving rats by the National Institute of Mental Health, the National Science Foundation and the Harry
and rabbits, I found the source from F. Guggenheim Foundation.
tivated by a neurotransmitter—glutamate to the cells at the peak of the theta wave, ically because it was not coding space. We
in this case. Glutamate momentarily opens LTP was induced. But if the same pulse continued recording from the two pairs of
a non-NMDA channel in the granule cell were applied at the trough of the waves— neurons as the rat moved about and then
dendrite, allowing sodium from the extra- or when theta rhythm was absent— LTP entered several sleep cycles. Six pairs of
cellular space to flow into the neuron. This was not induced. neurons were studied in this manner.
influx causes the granule cell to become A coherent picture of memory pro- We found that neurons that had cod-
depolarized. If the depolarization is suffi- cessing was emerging. As a rat explores, ed space fired at a normal rate as the ani-
cient, the granule cell fires, transmitting in- for example, brain stem neurons activate mal moved about prior to sleep. In sleep,
formation to other nerve cells. theta rhythm. Olfactory input (which in however, they fired at a significantly high-
was awake occurred in sleep at the level REM sleep, when dreaming occurs. tion had to be suppressed by inhibiting
of individual neurons. motor neurons. Suppressing eye move-
Bruce L. McNaughton and his col- Evolution of REM Sleep ment was unnecessary because this ac-
leagues at the University of Arizona have EVIDENCE THAT theta rhythm encodes tivity does not disturb sleep.
developed a technique for simultaneously memories during REM sleep may be de- Eye movement potentials, similar to
recording from a large number of neurons rived not only from neuroscientific stud- PGO spikes, accompany rapid eye move-
in the hippocampus that map locations. ies but also from evolution. The emer- ment in the waking state and also during
Their technique allows definitive patterns gence of a neural mechanism to process REM sleep. The function of these signals
of firing to be identified. In animal studies, memory in REM sleep suggests differ- has not yet been established, but they
they found that ensembles of place-field ences in brain anatomy between mam- may serve to alert the visual cortex to in-
MORE TO E XPLORE
CAROL DONNER (illustrations); GABOR KISS (chart)
Interspecies Differences in the Occurrence of Theta. Jonathan Winson Activity of These Cells during Subsequent Sleep Episodes. Constantine
in Behavioral Biology, Vol. 7, No. 4, pages 479–487; 1972. Pavlides and Jonathan Winson in Journal of Neuroscience, Vol. 9, No. 8,
Loss of Hippocampal Theta Rhythm Results in Spatial Memory Deficit pages 2907–2918; August 1989.
in the Rat. Jonathan Winson in Science, Vol. 201, No. 435, pages Dependence on REM Sleep of Overnight Improvement of a Perceptual
160–163; 1978. Skill. Avi Karni, David Tanne, Barton S. Rubenstein, Jean J. M. Askenasy
Brain and Psyche: The Biology of the Unconscious. Jonathan Winson. and Dov Sagi in Science, Vol. 265, pages 679–682; July 29, 1994.
Anchor Press, Doubleday, 1985. Reactivation of Hippocampal Ensemble Memories during Sleep.
Long-Term Potentiation in the Dentate Gyrus Is Induced Preferentially Mathew A. Wilson and Bruce L. McNaughton in Science, Vol. 265, pages
on the Positive Phase of Q-Rhythm. Constantine Pavlides, Yoram J. 676–679; July 29, 1994.
Greenstein, Mark Grudman and Jonathan Winson in Brain Research, Brain Gene Expression during REM Sleep Depends on Prior Waking
Vol. 439, pages 383–387; 1988. Experience. Sidarta Ribeiro, Vikas Goyal, Claudio V. Mello and Constantine
Influences of Hippocampal Place Cell Firing in the Awake State on the Pavlides in Learning and Memory, Vol. 6, pages 500–508; 1999.