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Brain Rhythmic Activities
Saturday, December 15 2012, 11:40 AM
Brain Rhythmic Activities
Citation: Steriade, Mircea (2004) Brain Rhythmic Activity, IBRO
History of
Neuroscience[http://www.ibro.info/Pub/Pub_Main_Display.asp?LC_Docs_ID=3160]Accessed:
(date)
Mircea Steriade
Brain Rhythmic Activity
Brain rhythms are defined as regularly recurring waves of
similar shape and frequency. They havebeen recognized since the
beginnings of electroencephalographic (EEG) recordings (Caton,
1875;Figure 1), and the alpha rhythm, which appears during the
state of relaxed wakefulness, has beenthoroughly described in
humans during the 1920s-1930s (Berger, 1929; Figure 2). However,
thedetailed mechanisms underlying EEG rhythms could be analyzed
only during the past four decadesand especially since 1980. This
was due to the advent of methods allowing the description
ofelectrophysiological properties and ionic currents in single
neurons investigated in vitro (Llinás,1988) and the network
operations that are responsible for the collective oscillations of
largeneuronal populations in the intact brain (Steriade, 2001).
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Figure 1 R. Caton
We know in detail the intrinsic neuronal properties and network
synchronization of spindleoscillation (7-14 Hz), which is generated
in the thalamus and characterizes the state of lightsleep, as well
as the cellular mechanisms underlying the more recently described
slow sleeposcillation (0.5-1 Hz) that is elaborated in the
neocortex. Both spindles and slow sleep oscillationsare associated
with prolonged inhibitory processes in thalamic and cortical
neurons, thus gatingincoming signals and preventing processing of
information from the outside world. We also havesome knowledge of
various brain structures and neuronal types generating beta and
gamma waves(20-60 Hz). There is, however, a continuous debate about
the significance of these fast rhythms,some claiming their role in
highly cognitive processes and consciousness during waking and
sleepwith rapid-eye-movements (REMs), others challenging this
hypothesis on the basis that the samerhythms also appear,
discontinuously, during slow-wave sleep or deep anesthesia
whenconsciousness is suspended (see Figure 3). The theta rhythm
(4-7 Hz), produced in thehippocampus and occurring during different
forms of arousal, especially in rodents, was studied atthe cellular
level, but its precise mechanisms are still subject to
controversies. Finally, eventhough alpha waves, with frequencies
overlapping those of spindle waves, have been repeatedlyreported
during the 1930s, we know virtually nothing about the underlying
neuronal mechanisms.
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Figure 2. H. Berger
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Figure 3
The important point is that, although various oscillations have
been demonstrated to arise withinthe thalamus or the cerebral
cortex, these structures are closely related (Jones, 1985) and
theirreciprocal connections account for interactions in
corticothalamic systems as well as thecoalescence of different
rhythms within complex sequences of waves (Steriade, 2003).
Forexample, although spindles can still be generated in the
thalamus of decorticated animals, thecorticothalamic feedback
controls the synchronization of these oscillations. Thus, in the
intactbrain, sequences of spindle waves occur simultaneously over
widespread thalamic and corticalterritories in animals and humans,
in contrast with their spatial disorganization in the absence
ofcortex (Contreras et al., 1996). At variance with the appearance
of distinct, isolated brainrhythms in structures of simplified
preparations, as is the case of brain slices, the cortical
slowoscillation has the virtue of grouping other sleep rhythms as
well as fast (beta and gamma) waves(Figure 3). This coalescence of
various oscillatory types, which can only be seen in
intactcorticothalamic systems, was described using multiple
intracellular and field potential recordings inanimals (Contreras
and Steriade, 1995; Steriade, 2004) and was confirmed in EEG
studies duringnatural night sleep in humans (Mölle et al.,
2002).
Some cortical neurons are preferentially implicated in
corticothalamocortical interactions, whichmay explain the grouping
of various low-frequency and high-frequency brain rhythms.
Amongthese neuronal types, fast-rhythmic-bursting (FRB) cells are
located throughout cortical layers IIto VI and fire bursts of
action potentials that recur rhythmically within the frequency
range ofbeta or gamma waves (20-40 Hz). The FRB neurons in deep
cortical layers project to the thalamusand, during both
brain-activated states (waking and REM sleep) or during the slow
sleeposcillation, they impact on thalamic circuitry. The integrated
thalamic activity is returned not onlyto cortical areas where the
inputs arise but also to distant cortical fields, due to thalamic
nucleiwith widespread cortical projections (Jones, 2001).
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The above data show that the study of brain rhythms during
behavioral states of vigilancerequires investigations conducted in
preparations with undamaged corticothalamic systems, whichoperate
under the control of different neuromodulatory systems. Any
procedure that interfereswith the normal intactness of these
structures may lead to false results. In the case of sleepspindles,
studies in vivo have demonstrated that their generator is located
within a peculiarthalamic nucleus, called reticular nucleus, which
uniquely consists of neurons that release apotent inhibitory
transmitter, the gamma aminobutyric acid (GABA). Although some
experiments invitro did not record spindles in the isolated
thalamic reticular nucleus, this failure was explained bythe
slicing procedure that cuts the long dendrites of thalamic
reticular neurons, which are cruciallyimportant in the generation
of this rhythm (Steriade et al., 1993). Another factor that should
betaken in consideration is the necessary condition that, to
produce spindles, thalamic reticularneurons should be excited by
projections from brainstem monoamine-containing (dorsal raphe
andlocus coeruleus) neurons or other activating systems, such the
cerebral cortex, which are absentin a thalamic slice.
What are the functions of brain rhythms? The spontaneous
oscillations have long been regarded asepiphenomena, with
negligible or no functional significance. This view may apply to
low-frequencyrhythms that define slow-wave sleep, because this
behavioral state was previously regarded asassociated with global
inhibition of the cerebral cortex and subcortical structures, which
underliesthe annihilation of consciousness. However, studies using
intracellular recordings ofelectrophysiologically characterized
cortical cell types in naturally awake and sleeping animals,showed
unexpectedly high levels of spontaneous neuronal activity during
slow-wave sleep(Steriade et al., 2001). And, though the thalamic
gates are closed for signals from the outsideworld during slow-wave
sleep, because of obliteration of synaptic transmission in
thalamocorticalneurons, the intracortical dialogue and
responsiveness of cortical neurons are maintained and evenincreased
during this quiescent state. These data suggest that slow-wave
sleep may serveimportant cerebral functions, among them the
consolidation of memory traces acquired duringwakefulness.
The first clear hypothesis relating states of vigilance, and in
particular sleep, with plastic activityin the cerebrum belongs to
Moruzzi (1966). He postulated that sleep does not concern the
fastrecovery processes in routine synapses underlying stereotyped
activities, but the slow recovery oflearned synapses. Since then,
the topics of synaptic plasticity and memory storage have
evolvedtoward analyses of neuronal networks in corticothalamic
systems by studying the effects of pulse-trains in the frequency
range of different waking and sleep rhythms on cortical and
thalamiccellular responsiveness (Steriade and Timofeev, 2003).
These and other animal studies (Buzsáki,1998; Frank et al., 2001)
led to the conclusion that spontaneous brain rhythms during
differentstates of vigilance may lead to increased responsiveness
and plastic changes in the strength ofconnections among neurons, a
mechanism through which information is stored. Human studieshave
also demonstrated that the overnight improvement of discrimination
tasks requires severalsteps, some of them depending on the early
stages of slow-wave sleep associated with spindlesand slow
oscillation (Stickgold et al., 2000; Hobson and Pace-Schott, 2002).
After training on adeclarative learning task, the density of human
sleep spindles is significantly higher, compared tothe non-learning
control task (Gais et al., 2002). All these data show that, far
from being a periodof complete inactivity, slow-wave sleep and the
associated brain rhythms are implicated in mentalprocesses. Indeed,
dreaming mentation appears closer to real life events during this
stage of sleep(Hobson et al., 2000) and the recall rate of dreaming
mentation in slow-wave sleep is high. Mircea SteriadeFaculty of
Medicine Laboratory of NeurophysiologyLaval UniversityQuebec,
Canada G1K [email protected]
Bibliography
-
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Buzsáki, G. (1998) Memory consolidation during sleep: a
neurophysiologicalperspective. J. Sleep Res. 7 (Suppl. 1):
17-23.
Caton, R. (1875) The electric currents of the brain. Br. Med. J.
2: 278.Berger, H. (1929) Über das Elektroencephalogramm des
Menschen. Arch. Psychiat. Nervenkr. 87:527-570.
Contreras, D. and Steriade, M. (1995) Cellular basis of EEG slow
rhythms: a study of dynamiccorticothalamic relationships. J.
Neurosci. 15: 604-622.
Contreras, D., Destexhe, A., Sejnowski, T.J. and Steriade, M.
(1996) Control of spatiotemporalcoherence of a thalamic oscillation
by corticothalamic feedback. Science 274: 771-774.
Frank, M.G., Issa, N.P. and Stryker, M.P. (2001) Sleep enhances
plasticity in thedeveloping visual cortex. Neuron 30: 275-287.
Gais, S., Mölle, M., Helms, K. and Born, J. (2002)
Learning-dependent increases in sleep density. J.Neurosci. 22:
6830-6834.
Hobson, J.A. and Pace-Schott, E.F. (2002) The cognitive
neuroscience of sleep: neuronalsystems, consciousness and learning.
Nat. Rev. Neurosci. 3: 679-693.
Hobson, J.A., Pace-Schott, E. and Stickgold, R. (2000) Dreaming
and the brain: toward a cognitiveneuroscience of conscious states.
Brain Behav. Sci. 23: 793-842.
Jones, E.G. (1985) The Thalamus. New York: Plenum.
Jones, E.G. (2001) The thalamic matrix and thalamocortical
synchrony. Trends Neurosci 24:595-601.
Llinás, R.R. (1988) The intrinsic electrophysiological
properties of mammalian neurons: insights intocentral nervous
system function. Science 242: 1654-1664.
Mölle, M., Marshall, L., Gais, S. and Born, J. (2002) Grouping
of spindle activity during slowoscillations in human non-REM sleep.
J. Neurosci. 22: 10941-10947.
Moruzzi, G. (1966) The functional significance of sleep with
particular regard to the brainmechanisms underlying consciousness.
In Brain and Conscious Experience, J.C. Eccles, ed., pp.345-379.
New York: Springer.
Steriade, M. (2001) The Intact and Sliced Brain. Cambridge (MA):
MIT Press.
Steriade, M. (2003) Neuronal Substrates of Sleep and Epilepsy.
Cambridge (UK): Cambridge Univ.Press.
Steriade, M. (2004) Neocortical cell classes are flexible
entities. Nature Rev. Neurosci. 5: 121-134.
Steriade, M. and Timofeev, I. (2003) Neuronal plasticity in
thalamocortical networks during sleepand waking oscillations.
Neuron 37: 563-576.
Steriade, M., McCormick, D.A. and Sejnowski, T.J. (1993)
Thalamocortical oscillation in thesleeping and aroused brain.
Science 262: 679-685.
Steriade, M., Amzica, F. and Contreras, D. (1996)
Synchronization of fast (30-40 Hz) spontaneouscortical rhythms
during brain activation. J. Neurosci. 16: 392-417.
Steriade, M., Timofeev, I. and Grenier, F. (2001) Natural waking
and sleep states: a view from
-
12/15/12 Ev ernote Web
7/7https://www.ev ernote.com/edit/147507d6-68b0-4f
68-b2a0-817c2809bacd#st=p&n=147507d6-68b0-4…
inside neocortical neurons. J. Neurophysiol. 85: 1969-1985.
Stickgold, R., James, L. and Hobson, J.A. (2000) Visual
discrimination learning requires sleep aftertraining. Nat.
Neurosci. 3: 1237-1238
Originally published on 2005-07-08