Regional cerebral blood flow correlates with heart period and high‐frequency heart period variability during working‐memory tasks: Implications for the cortical and subcortical regulation of cardiac autonomic activity

Abstract

The aim of the present study was to characterize the functional relationships between behaviorally evoked regional brain activation and cardiac autonomic activity in humans. Concurrent estimates of regional cerebral blood flow (rCBF; obtained by positron emission tomography), heart period, and high-frequency heart period variability (HFHPV; an indicator of cardiac parasympathetic activity) were examined in 93 adults (aged 50-70 years) who performed a series of increasingly difficult working-memory tasks. Increased task difficulty resulted in decreased heart period (indicating cardioacceleration) and decreased HF-HPV (indicating decreased cardiac parasympathetic activity). Task-induced decreases in heart period and HF-HPV were associated with concurrent increases and decreases in rCBF to cortical and subcortical brain regions that are speculated to regulate cardiac autonomic activity during behavioral processes: the medialprefrontal, insular, and anterior cingulate cortices, the amygdala-hippocampal complex, and the cerebellum. These findings replicate and extend a small number of functional neuroimaging studies that suggest an important role for both cortical and subcortical brain systems in human cardiac autonomic regulation. KeywordsCentral cardiac autonomic regulation; Heart period; High-frequency heart period variability; Positron emission tomography The cortical and subcortical brain systems that regulate cardiac autonomic activity during behavior have been detailed by extensive research in nonhuman animals (reviewed by Bennarroch, 1997;Buchanan & Powell, 1993;Loewy & Spyer, 1990 NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptHurley, Ruit, & Frysztak, 1993). An open question is whether similar brain systems regulate behaviorally integrated cardiac autonomic activity in humans. Answering this question is important because the brain's regulation of cardiac autonomic activity is purported to influence a range of behavioral processes: attending to novel stimuli (Porges, 1995), processing environmental information (Lacey & Lacey, 1974), making decisions (Damasio, 1994), experiencing fear and anxiety (Berntson, Sarter, & Cacioppo, 1998), perceiving pain (Dworkin et al., 1994;Rosen et al., 1996), and reacting to stressors (Lovallo & Gerin, 2003) are examples of such processes.Drawing on the support of nonhuman animal research, the cortical brain systems that are hypothesized to regulate cardiac autonomic activity during behavior include the medialprefrontal (Brodmann Areas 10 and 11), insular, and anterior cingulate (Brodmann Areas 24, 25, and 32) regions of the cortex. A prevailing view is that these cortical systems act as a network with subcortical systems to initiate and represent cardiac autonomic adjustments that support behavioral responses to environmental, psychological, and social stimuli (Bennarroch, 1997;Cechetto, 1994;Groenewegen & Uylings, 2000;Loewy & Spyer, 1990;Thayer & Lane, 2000). Subcortical regions that are thought to regulate behaviorally integrated cardiac ...

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“…Gianaros et al covaried HF with H 2 15 O PET during graded memory tasks (Gianaros et al 2004) and found that regional cerebral blood flow (rCBF) covaried positively with HF in the right VMPFC, left insula, and left amygdala-hippocampal complex, while covarying negatively in the right cerebellum. Lane et al similarly covaried HF with PET neuroimaging during an emotion-laden task (Lane et al 2001).…”

“…Several groups have attempted to relate estimates of efferent autonomic activity using HF power with concurrent brain response using Positron Emission Tomography (PET) (Lane et al 2001;Gianaros et al 2004) or functional Magnetic Resonance Imaging (fMRI) (Critchley et al 2003;Napadow et al 2005) during behavioral tasks that are thought to modulate the ANS. Correlating fMRI task response with out-of-scanner baseline HF (O'Connor et al 2007) or HF response to the in-scanner task (Matthews et al 2004) has also been performed.…”

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“…Sympathetic activity, as measured by pupillary dilation (Critchley et al, 2005) and skin conductance responses (Nagai et al, 2004), have both been correlated with neural activation in the anterior cingulate cortex (ACC). Parasympathetic activity, as measured by the highfrequency component of heart rate variability, has also been associated with the ACC during fMRI tasks involving working memory and emotion (Gianaros et al, 2004;Lane et al, 2001;Matthews et al, 2004). The demonstrated relationship between autonomic activity indicative of arousal and ACC activity is consistent with the dense projections from the ACC to cell groups that regulate autonomic functions, such as the amygdala, hypothalamus, and brainstem nuclei (Neafsey et al, 1993).…”