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The Journal of Neuroscience, September 16, 2009, 29(37):11698-11707; doi:10.1523/JNEUROSCI.5773-08.2009

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Behavioral/Systems/Cognitive
Basal Forebrain Lactate Release and Promotion of Cortical Arousal during Prolonged Waking Is Attenuated in Aging

Henna-Kaisa Wigren, Kirsi-Marja Rytkönen, and Tarja Porkka-Heiskanen

Institute of Biomedicine/Physiology, Biomedicum Helsinki, University of Helsinki, FIN-00014 Helsinki, Finland

Correspondence should be addressed to Dr. Henna-Kaisa Wigren, Institute of Biomedicine/Physiology, Biomedicum Helsinki, University of Helsinki, P.O. Box 63, FIN-00014 Helsinki, Finland. Email: henna-kaisa.wigren{at}helsinki.fi

The wake-promoting basal forebrain (BF) is critically involved in sustaining cortical arousal. In the present study, we investigated how aging affects the capacity of the BF to cope with continuous activation during prolonged waking. Increased neuronal activity induces lactate release in the activated brain area, and BF stimulation increases cortical arousal. We used in vivo microdialysis to measure lactate levels in the BF, and electroencephalography (EEG) to measure cortical arousal, during 3 h sleep deprivation (SD) in three age groups of rats. Lactate increased during SD in young but not in aged (middle-aged and old) rats. The increase in high-frequency (HF) EEG theta power (7–9 Hz), a marker of cortical arousal and active waking, was attenuated in the aged. Furthermore, a positive correlation between BF lactate release and HF EEG theta increase was found in young but not in aged rats. We hypothesized that these age-related attenuations result from reduced capacity of the BF to respond to increased neuronal activation. This was tested by stimulating the BF with glutamate receptor agonist NMDA. Whereas BF stimulation increased waking in young and old rats, lactate increase and the HF EEG theta increase were attenuated in the old. Also, the homeostatic increase in sleep intensity after SD was attenuated in aged rats. Our results suggest that an age-related attenuation in BF function reduces cortical arousal during prolonged waking. As the quality of waking is important in regulating the subsequent sleep, reduced cortical arousal during SD may contribute to the age-related reduction in sleep intensity.

Received Dec. 3, 2008; revised July 23, 2009; accepted Aug. 8, 2009.

Correspondence should be addressed to Dr. Henna-Kaisa Wigren, Institute of Biomedicine/Physiology, Biomedicum Helsinki, University of Helsinki, P.O. Box 63, FIN-00014 Helsinki, Finland. Email: henna-kaisa.wigren{at}helsinki.fi






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