The Journal of Neuroscience, February 11, 2009, 29(6):1817-1825; doi:10.1523/JNEUROSCI.3363-08.2009
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Behavioral/Systems/Cognitive
Following One's Heart: Cardiac Rhythms Gate Central Initiation of Sympathetic Reflexes
Marcus A. Gray,1,2
Karin Rylander,4
Neil A. Harrison,3
B. Gunnar Wallin,4 and
Hugo D. Critchley1
1Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex, Brighton, East Sussex BN1 9RR, United Kingdom, 2Wellcome Trust Centre for Neuroimaging, University College London, London WC1N 3BG, United Kingdom, 3Institute of Cognitive Neuroscience, University College London, London WC1N 3AR, United Kingdom, and 4Institute of Neuroscience and Physiology, Department of Clinical Neurophysiology, Sahlgren University Hospital, SE-413 45 Gothenburg, Sweden
Correspondence should be addressed to Marcus A. Gray, Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex, Brighton, East Sussex BN1 9RR, UK. Email: m.a.gray{at}bsms.ac.uk
Central nervous processing of environmental stimuli requires integration of sensory information with ongoing autonomic control of cardiovascular function. Rhythmic feedback of cardiac and baroreceptor activity contributes dynamically to homeostatic autonomic control. We examined how the processing of brief somatosensory stimuli is altered across the cardiac cycle to evoke differential changes in bodily state. Using functional magnetic resonance imaging of brain and noninvasive beat-to-beat cardiovascular monitoring, we show that stimuli presented before and during early cardiac systole elicited differential changes in neural activity within amygdala, anterior insula and pons, and engendered different effects on blood pressure. Stimulation delivered during early systole inhibited blood pressure increases. Individual differences in heart rate variability predicted magnitude of differential cardiac timing responses within periaqueductal gray, amygdala and insula. Our findings highlight integration of somatosensory and phasic baroreceptor information at cortical, limbic and brainstem levels, with relevance to mechanisms underlying pain control, hypertension and anxiety.
Key words: baroreceptor; blood pressure; PAG; amygdala; insula; fMRI; shock; anxiety; blood phobia; HF HRV
Received July 18, 2008;
revised Dec. 4, 2008;
accepted Dec. 7, 2008.
Correspondence should be addressed to Marcus A. Gray, Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex, Brighton, East Sussex BN1 9RR, UK. Email: m.a.gray{at}bsms.ac.uk