Brain Advance Access originally published online on November 1, 2006
Brain 2006 129(12):3343-3355; doi:10.1093/brain/awl299
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Right ventromedial prefrontal lesions result in paradoxical cardiovascular activation with emotional stimuli
1 Department of Neurology, New York University New York, NY, USA 2 Department of Neurology, Mount Sinai School of Medicine New York, NY, USA 3 Department of Psychology, Queens College and The Graduate Center of the City University of New York (CUNY) New York, NY, USA 4 Department of Neurology, University of Erlangen-Nuremberg, Erlangen Germany 5 Department of Neurology, Jagiellonian University Medical College Cracow, Poland
Correspondence to: Orrin Devinsky, MD, Comprehensive Epilepsy Center, New York University School of Medicine, 403 East 34th Street, 4FL; New York, NY 10016, USA E-mail: od4{at}nyu.edu
Ventromedial prefrontal cortex (VMPFC) lesions can alter emotional and autonomic responses. In animals, VMPFC activation results in cardiovascular sympathetic inhibition. In humans, VMPFC modulates emotional processing and autonomic response to arousal (e.g. accompanying decision-making). The specific role of the left or right VMPFC in mediating somatic responses to non-arousing, daily-life pleasant or unpleasant stimuli is unclear. To further evaluate VMPFC interaction with autonomic processing of non-stressful emotional stimuli and assess the effects of stimulus valence, we studied patients with unilateral VMPFC lesions and assessed autonomic modulation at rest and during physical challenge, and heart rate (HR) and blood pressure (BP) responses to non-stressful neutral, pleasant and unpleasant visual stimulation (VES) via emotionally laden slides. In 6 patients (54.0 ± 7.2 years) with left-sided VMPFC lesions (VMPFC-L), 7 patients (43.3 ± 11.6 years) with right-sided VMPFC lesions (VMPFC-R) and 13 healthy volunteers (44.7 ± 11.6 years), we monitored HR as R–R interval (RRI), BP, respiration, end-tidal carbon dioxide levels, and oxygen saturation at rest, during autonomic challenge by metronomic breathing, a Valsalva manoeuvre and active standing, and in response to non-stressful pleasant, unpleasant and neutral VES. Pleasantness versus unpleasantness of slides was rated on a 7-point Likert scale. At rest, during physical autonomic challenge, and during neutral VES, parameters did not differ between the patient groups and volunteers. During VES, Likert scores also were similar across the three groups. During pleasant and unpleasant VES, HR decreased (i.e. RRI increased) significantly whereas BP remained unchanged in volunteers. In VMPFC-L patients, HR decrease was insignificant with pleasant and unpleasant VES. BP slightly increased (P = 0.06) with pleasant VES but was stable with unpleasant VES. In contrast, VMPFC-R patients had significant increases in HR and BP during pleasant and not quite significant HR increases (P = 0.06) with only slight BP increase during unpleasant VES. Other biosignals remained unchanged during VES in all groups. Our results show that VMPFC has no major influence on autonomic modulation at rest and during non-emotional, physical stimulation. The paradoxical HR and BP responses in VMPFC-R patients suggest hemispheric specialization for VMPFC interaction with predominant parasympathetic activation by the left, but sympathetic inhibition by the right VMPFC. Valence of non-stressful stimuli has a limited effect with more prominent left VMPFC modulation of pleasant and more right VMPFC modulation of unpleasant stimuli. The paradoxical sympathetic disinhibition in VMPFC-R patients may increase their risk of sympathetic hyperexcitability with negative consequences such as anxiety, hypertension or cardiac arrhythmias.
Key Words: cardiovascular autonomic system; emotion; prefrontal cortex; somatic markers; valence hypothesis
Abbreviations: BP, blood pressure; HR, heart rate; RRI, R–R interval; VMPFC, ventromedial prefrontal cortex; VMPFC-L, left-sided VMPFC lesions; VMPFC-R, right-sided VMPFC lesions
Received January 19, 2006. Revised August 20, 2006. Accepted September 22, 2006.
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