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J Physiol Volume 578, Number 2, 605-612, January 15, 2007 DOI: 10.1113/jphysiol.2006.122549
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INTEGRATIVE

Identifying cardiorespiratory neurocircuitry involved in central command during exercise in humans

Alexander L. Green1,2, Shouyan Wang1, Sarah Purvis1, Sarah L. F. Owen1, Peter G. Bain3, John F. Stein1, Abe Guz1,4, Tipu Z. Aziz1,2 and David J. Paterson1

1 Department of Physiology, Anatomy and Genetics, University of Oxford, Sherrington Building, Parks Road, Oxford OX1 3PT, UK
2 Department of Neurosurgery, Radcliffe Infirmary, Oxford OX2 6HE, UK
3 Division of Neurosciences and Mental Health, Imperial College London, Charing Cross Campus, Fulham Palace Road, London W6 8RF, UK
4 National Heart and Lung Institute, Charing Cross Campus, Imperial College School of Medicine, Fulham Palace Road, London W6 8RF, UK

For almost one hundred years, the exact role of human brain structures controlling the cardiorespiratory response to exercise (‘central command’) has been sought. Animal experiments and functional imaging studies have provided clues, but the underlying electrophysiological activity of proposed relevant neural sites in humans has never been measured. In this study, local field potentials were directly recorded in a number of ‘deep’ brain nuclei during an exercise task designed to dissociate the exercise from peripheral feedback mechanisms. Several patient groups had electrodes implanted sterotaxically for the treatment of movement disorder or chronic pain. Fast Fourier transform analysis was applied to the neurograms to identify the power of fundamental spectral frequencies. Anticipation of exercise resulted in increases in heart rate, blood pressure and ventilation. The greatest neural changes were found in the periaqueductal grey area (PAG) where anticipation of exercise was accompanied by an increase of 43% in the power of the 12–25 Hz frequency band (P = 0.007). Exercise increased the activity by 87% compared to rest (P = 0.006). Changes were also seen in the 60–90 Hz band when anticipation or exercise increased power by 32% (P = 0.006) and 109% (P < 0.001), respectively. In the subthalamic nucleus there was a reduction in the power of the beta frequency during both anticipation (7.6 ± 0.68% P = 0.001) and exercise (17.3 ± 0.96% P < 0.001), whereas an increase was seen with exercise only at higher frequencies (93 ± 1.8% P = 0.007). No significant changes were seen in the globus pallidus during anticipation of exercise. We provide direct electrophysiological evidence highlighting the PAG as an important subcortical area in the neural circuitry of the cardiorespiratory response to exercise, since stimulation of this structure is known to alter blood pressure in awake humans.

(Received 9 October 2006; accepted after revision 26 October 2006; first published online 2 November 2006)
Corresponding author A. L. Green: Department of Neurosurgery, Radcliffe Infirmary, Oxford OX2 6HE, UK. Email: alex.green{at}physiol.ox.ac.uk & D. J. Paterson: Department of Physiology, Anatomy and Genetics, Oxford, OX1 3PT, UK. Email: david.paterson{at}physiol.ox.ac.uk




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