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Brain Rhythmic Activities

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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).



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.

Figure 2. H. Berger


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).



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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Originally published on 2005-07-08

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