Download REM sleep and amygdala

Molecular Psychiatry (1997) 2, 195–196
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REM sleep and amygdala
Recent PET data on human sleep suggest functional interactions between the amygdala and
the cortex during REM sleep. This amygdalo-cortical interplay might reflect the processing of
some types of memory traces.
In humans, rapid eye movement (REM) sleep occurs
in short periods recurring at regular intervals, mainly
during the second half of the night. It is characterized
by low-amplitude fast-frequency EEG waves, bursts of
ocular saccades and muscular atonia. It is also strongly
associated with dreaming. Since its discovery in the
1950s by Aserinky and Kleitman1 as well as Jouvet,2
REM sleep has been intensively investigated and a
huge body of data has been collected in animals concerning its generation and maintenance at the cellular
level.3 In short, cholinergic nuclei from the mesopontine reticular formation, liberated from the serotoninergic and noradrenergic inhibition, tonically activate
the thalamic nuclei. In turn, these stimulate cortical
areas. In particular, intralaminar thalamic nuclei project over and stimulate widespread cortical fields. This
important neuronal activity explains why the global
level of energy metabolism during REM sleep is comparable to the waking level.4,5 What is barely known is
whether this diffuse telencephalic activation is homogeneous or not. In other words, the distribution of neuronal activity at the telencephalic level during REM
sleep remains largely unexplored, especially in
humans.
Previous reports using PET or SPECT did not succeed in sketching a consistent metabolic pattern during
REM sleep. Some authors described a significant metabolic increase in cingulate gyrus, corpus callosum and
optic radiations. 6 Others observed an activation of posterior (occipital and temporal) areas during REM sleep,
a metabolic pattern that was putatively attributed to
dreaming activity.4,7 With the technological progress in
PET methodology (H215O technique) and in data analysis (Statistical Parametric Mapping, SPM8), it has
recently been possible to localize brain areas, whose
activity characterizes REM sleep in humans.9 Experimental data show that some areas are more—and others
less—activated than the rest of the brain. Not unexpectedly, an activation of dorsal pontine tegmentum and
of thalamic nuclei was observed, consistent with data
Correspondence: Dr P Maquet, Cyclotron Research Center (B30)
and Department of Neurology, University of Liege, 4000 Liege,
Belgium. E-mail: maquetKpet.crc.ulg.ac.be
obtained in animals. More rostrally, an unexpected
activation is shown in both amygdaloid complexes.
Moreover, the distribution of cortical activity suggests
that functional relationships take place between amygdala and the cortex during REM sleep. Indeed, significantly activated cortical areas (anterior cingulate cortex, parietal operculum) all receive a sizeable number
of amygdalar connections (as can be inferred from what
is known in primate neuroanatomy10) whereas the
cortical regions with few or no amygdala afferents are
significantly less active than the rest of the brain
(prefrontal areas, parietal cortex, precuneus). From
these results, one could speculate that, during REM
sleep, the diffuse global activation of the cortex by central core structures (mesopontine reticular formation
and thalami) is modulated by the amygdala.
These results may further help to formulate some
working hypotheses. First, amygdaloid complexes are
known to associate an affective content to perceptions.11 They are also deeply involved in affective
memory and experimental data further suggest that
amygdala would modulate memory storage in other
brain regions.12 On the other hand, both in animals and
in man, REM sleep periods were shown to influence
the consolidation of (mainly procedural) memory
tasks.13 Taken together, these data suggest that the beneficial effect of REM sleep on some type of memory
might, at least in part, rely on the modulation by amygdala of memory storage in other brain areas.
Second, since all subjects recalled a dream after each
REM sleep scan, these results also shed some light on
the neural correlates of dreaming.14 One can speculate
that the activation of the amygdala and anterior cingulate cortex could account for the emotional aspects of
dreaming. The relative deactivation of some prefrontal
areas could explain some of the aspects of dreams
related to the loss of executive prefrontal functions:
absence of strategy, poor critical introspection, distortion of temporal scale, amnesia upon awakening. The
perceptual aspects of dreams would be brought about
by the activation of various posterior cortices.
Third, this study might provide some clues concerning the neural substrate of REM sleep disturbances in
various pathologies such as narcolepsy and depression,
News & Views
196
in which an amygdalar dysfunction has already been
suggested. 15,16
There is still a lot of work to be done to test all these
hypotheses in humans. However, we are confident that
studies using coregistered functional neuroimaging
techniques may be able to approach these questions in
the near future.
P Maquet, G Franck
Cyclotron Research Center (B30)
and Department of Neurology
University of Liège
4000 Liège, Belgium
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