A EEG Arousal Is Controlled by Interconnections between the NMTs Thalamus and Cortex

1. Two Modes of Thalamic Activity

Changes in the EEG during arousal are produced by an interaction of the NMTs with the cortex and thalamus. The NMTs control the strength and pattern of the coupling between the thalamus and the cortex.

During rest or sleep, thalamic reticular neurons (Fig. 1) emit rhythmic bursts of action potentials within a narrow range of frequencies (4-8 Hz). The bursting pattern is maintained as long as these cells are slightly

Cortical Arousal Eeg

Figure 1 (A) Early model of arousal systems, circa 1972. The RF was considered a unitary structure that modified processing in sensory thalamic relay structures, nonsensory diffuse nuclei, and the cortex. The two groups of thalamic nuclei were mutually interconnected. (B) Contemporary view of arousal systems. Each NMT (bottom) sends influences to both the RT and the TRN. The RT contains oscillatory circuits (dotted line) that produce the rhythmic activity of the brain. (C) Electrical activity recorded in the cortex and the effects of electrical stimulation (tetanus) of the cholinergic NBM. The EEG switches from high-voltage slow waves to low-voltage fast activity. Individual cells show burst activity prior to tetanus and single spike activity for several seconds after tetanus [reproduced with permission from Metherate et al., (1992). J. Neurosci. 12, 47014711. Copyright Society for Neuroscience]. RF, reticular formation; NBM, basal nucleus of Meynert; PPT, peduncolopontine tegmental nucleus; LC, locus coeruleus; RT, relay thalamic nucleus; SN/VTA, substantia nigra/ventral tegmental nuclei; TMH, tuberomamillary hypothalamic nucleus; DR, dorsal raphe nucleus; TRN, thalamic reticular nucleus.

hyperpolarized. Hyperpolarization may be caused by the release of SE in the thalamus by the brain stem raphe nuclei. Thalamic burst activity, known as the burst mode, is relayed to the cortex, where it produces cortical burst activity. On the scalp, this pattern is recorded as high-voltage, slow-wave cortical activity, known as the synchronized EEG.

In contrast, the low-voltage, fast-wave activity, known as the desynchronized EEG, results when NMTs suppress the hyperpolarizing influences on thalamic neurons and shift the thalamic activity into the single-spike mode. This activity is initiated by ACH that is released from the terminals of basal forebrain neurons. The frequency spectrum of rhythmic activity increases substantially and high frequencies (40-60 Hz) may be frequent. Similar patterns are engendered in cortical neurons and the EEG records of this activity are seen during REM sleep and waking states. Although high-frequency EEG activity has been characterized as desynchronized, it may simply be synchronized to higher frequencies. The mechanisms underlying the burst and single-spike mode are discussed in-depth later.

2. Models of NMT Modulation of Thalamocortical Activity

The mechanisms underlying EEG desynchronization have been of great interest for decades. Early studies in the 1940s and 1950s by Moruzzi and Magoun and others showed that stimulation of the midline thalamus caused a desynchronized EEG pattern in anesthetized cats. Based on these results, two systems for the control of cortical arousal were hypothesized: the generalized thalamocortical system, composed of the midline and intralaminar thalamic nuclei, and the specific (relay) thalamocortical system. The relay system carries sensory information to the cortex, but its cortical influence is modulated by the generalized system. The general system has also been called the ascending reticular system and the diffuse thalamocortical projection system.

The arousal systems must work in unison to control behavior, but the arousal response is not necessarily stereotyped. In some circumstances, the EEG and other indices of arousal may be uncorrelated with behavioral or physiological responses. Specific behavioral contexts are important in determining the patterns of motor, autonomic, emotional responses. For example, intense fear may cause overt, widespread changes in muscular locomotor activity and produce escape responses. Alternatively, there may be a complete lack of overt activity but widespread covert changes in muscle tone, such as occurs during "freezing" behavior. These qualitative changes may indicate an underlying shift in dominance from one transmitter system to another. Thus, it is more appropriate to view arousal as a flexible response to changing environmental demands rather than as a reflexive, fixed pattern of activity.

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