[Frontiers in Bioscience 8, s438-451, May 1, 2003]

AROUSAL SYSTEMS

Barbara E. Jones

Department of Neurology and Neurosurgery, McGill University, Montreal Neurological Institute, Montreal, Quebec, Canada H3A 2B4

TABLE OF CONTENTS

1. Abstract
2. Introduction
3. Brainstem arousal systems
3.1. The reticular formation
3.2. The cholinergic ponto-mesencephalic neurons
3.3. The noradrenergic locus coeruleus neurons
3.4. The dopaminergic ventral mesencephalic neurons
3.5. The serotonergic raphe neurons
4. Thalamo-cortical activating system
5. Hypothalamic arousal systems
5.1. The posterior hypothalamus
5.2. The histaminergic tuberomammillary neurons
5.3. The orexinergic peri-fornical neurons
6. Basal forebrain interleaved wake and sleep promoting systems
6.1. The cholinergic basal forebrain neurons
6.2. The non-cholinergic basal forebrain neurons
7. Conclusions and Perspective
8. Acknowledgements
9. References

1. ABSTRACT

The brain contains autochthonous neural systems that evoke waking from sleep in response to sensory stimuli, prolong or enhance arousal in response to special stimuli, and also generate and maintain wakefulness regardless of sensory stimuli during the active part of the day. Through ascending projections to the cortex, these arousal systems stimulate cortical activation, characterized by high frequency gamma and low frequency rhythmic theta activity, and through descending projections to the spinal cord, they stimulate muscle tonus along with sensory-motor responsiveness and activity. They are comprised of neuronal aggregates within the brainstem reticular formation, thalamus, posterior hypothalamus and basal forebrain, and they utilize multiple different neurotransmitters. Within the brainstem, neurons of the reticular formation, which predominantly utilize glutamate as a neurotransmitter, stimulate cortical activation by exciting the widespread projecting neurons of the nonspecific thalamo-cortical projection system, which similarly utilize glutamate, and neurons of the ventral extra-thalamic relay systems located in the posterior hypothalamus and basal forebrain, many of which also utilize glutamate. In addition, these systems have descending projections by which they can enhance or modulate muscle tonus and activity. Articulating with these are cholinergic neurons of the ponto-mesencephalic tegmentum and basal forebrain that promote cortical activation during waking and also during rapid eye movement sleep (REMS), in association therein with muscle atonia. Dopaminergic ventral mesencephalic neurons stimulate a highly motivated and positively rewarding state during waking and may also do so during REMS. In contrast, noradrenergic locus coeruleus neurons promote an aroused waking state and prevent REMS as well as slow wave sleep (SWS). Serotonergic raphe neurons promote a seemingly quiet or satiated waking state, which though exclusive of REMS, can actually be conducive to SWS. Histaminergic neurons of the posterior hypothalamus act like noradrenergic neurons in enforcing waking and are joined by neurons in the region that contain orexin, a neuropeptide recently shown to maintain waking and in absentia to be responsible for narcolepsy, or the inability to maintain wakefulness. These multiple arousal systems are grossly redundant, since no one system is absolutely necessary for the occurrence of waking; yet they are differentiated, since each plays a special role in waking and sleep. During SWS, they are submitted to an inhibitory influence arising in part at least from particular GABAergic neurons co-distributed with many neurons of the arousal systems and also concentrated within the basal forebrain and adjacent preoptic region.