Barbara E. Jones, Ph.D.
Montreal Neurological Institute
Montreal, Quebec, Canada
November 1, 2010
Neural Systems Controlling Sleep-Wake States
Structure is not only found in terms of neurotransmitters, connections and circuits but also in the more abstract patterns to which these components give rise. The structure or form of activity across the brain is often seen to follow an oscillatory pattern, commonly referred to as brain waves. Importantly, the frequency of these patterns seems to change across differing behavioral contexts. Perhaps the most striking example of behavioral changes stemming from brain wave patterns is seen when examining the difference between the sleep and awake states. For this reason, we were delighted to hear from Dr. Barbara Jones, whose lab examines how these patterns are modulated by distinct groups of neurons.
All mammals and birds display three distinct states: waking, slow wave sleep (SWS) and rapid eye movement (REM) sleep. These three states are distinguished by electroencephalographic (EEG) and electromyographic (EMG) imaging techniques, as well as behavioral characteristics. Waking is characterized by high-frequency (gamma) EEG activity together with high postural muscle tone on the EMG, while slow wave sleep is characterized by low-frequency (delta) EEG activity, along with reduced muscle tone. REM sleep, paradoxically, can be characterized by high frequency (gamma) EEG activity (like waking) together with postural muscle atonia, typifying deep sleep. Different neural cell groups that contain distinct neurotransmitters and project to different targets that influence EEG or EMG can play different roles in these states. Discovering their discharge profiles across the sleep-wake cycle can reveal the way in which they generate or modulate sleep-wake states and their polygraphic features.
By applying juxtacellular recording and labeling of neurons in naturally sleeping-waking rats, the Jones Lab has been able to determine the discharge profile of several different identified neuronal populations across the sleep-waking cycle in association with EEG and EMG activity. In the basal forebrain, cholinergic neurons discharge in association with fast (gamma) EEG activity during both waking and REM sleep, and thus in association with cortical activation, independent of muscle tone. Glutamatergic and GABAergic neurons are also present in the same region and are differentiated according to their discharge profiles and thus their putative roles. Four functional sets or pairs of glutamatergic, with cholinergic and GABAergic neurons, could be distinguished: (1) the W/PS group, which includes cholinergic neurons and discharges with cortical activation during waking states and REM sleep; (2) the slow wave sleep group, which discharges with cortical slow wave activity during slow wave sleep; (3) the REM group, which discharges with muscle atonia during REM sleep; and (4) the waking group, which discharges with muscle tone and behavioral arousal during waking. These sets or pairs of excitatory/inhibitory neurons can function in an oscillatory manner through balanced excitation and inhibition. Through projections to the cerebral cortex, the waking/REM sleep and slow wave sleep groups modulate EEG activity across the sleep-wake cycle through projections to the cerebral cortex, while the REM sleep and waking groups are able to modulate EMG activity across the sleep-wake cycle via projections that influence the brainstem and spinal cord. Through interconnections between these circuits, different cell groups can oscillate to generate alternating EEG and EMG activities that characterize the three sleep-wake states. Other neuromodulatory systems can then further influence these circuit-level dynamics, and thus influence the resulting behavior.