Volitional Control of Autonomic Arousal: A Functional Magnetic Resonance Study

Abstract

Electrodermal activity reflects autonomic sympathetic innervation of dermal sweat glands providing an index of emotion-related bodily states of arousal. Relaxation techniques, which are facilitated by external (bio)feedback of electrodermal activity, can be used by trained subjects to actively control bodily and emotional arousal. Biofeedback relaxation provides an experimental model to explore neural mechanisms contributing to emotional representations and intentional autonomic control. We used functional magnetic resonance imaging (fMRI) to explore neural mechanisms contributing to integration of volitional intent, self-representation, and autonomic states of arousal, embodied within performance of a biofeedback relaxation exercise. Data were obtained from 17 subjects to assess brain activity during relaxation in which a visual index of electrodermal arousal was modulated by accuracy (addition of random "noise") or sensitivity (by scalar adjustments of feedback). A central matrix of cortical, subcortical and brainstem autonomic centres was activated during biofeedback relaxation, as well as regions that mediate visual and somatesthetic representations and executive control. Anterior cingulate, amygdala, and insula activity was modulated by task manipulations that increased demand on processing interoceptive representations, while variation in anterior insula activity reflected an interaction between accuracy and sensitivity of feedback. These findings identify neural substrates that support integration of perceptual processing, interoception, and intentional modulation of bodily states of arousal.

Effects of emotion regulation strategy on brain responses to the valence and social content of visual scenes

“…This interpretation is corroborated by the main effects of NEG > POS and NSOC > SOC that both revealed significant activations in the insula (Tables 1 and 2). Thus, our results demonstrate that both REAP and ESUP strategies produced a convergent modulatory effect on emotional processing of nonsocial aversive information in the insula, a brain area known to play a central role in the autonomic and subjective dimensions of affective responses (Critchley et al, 2002).…”

“…Negative images (compared to positive) increased activity mainly in right insula, prefrontal and parietal cortex, dorsal anterior cingulate, and extrastriate visual cortex, all brain areas known to be involved in arousal, attention, and object recognition (Critchley, Melmed, Featherstone, Mathias, & Dolan, 2002;Kim & Hamann, 2007;Vuilleumier, Armony, Driver, & Dolan, 2001;Vuilleumier, Richardson, Armony, Driver, & Dolan, 2004). Positive images produced greater activation in subgenual anterior cingulate cortex, hippocampus, and occipital regions (see Table 2 and Fig.…”

“…Insula responses are specifically linked to the affective, but not sensory, components of pain (Singer et al, 2004). Moreover, its activation reflects the degree of bodily arousal evoked by NEG stimulus content, which might interface cognitive control with changes in autonomic responses during ER (Critchley et al, 2002). Because NEG scenes in our study often displayed people experiencing pain or distressing conditions (SOC category), as well as situations representing harmful or disgust conditions (NSOC category), the decreases in aINS activation might be interpreted as a reduction of the affective component of empathic responses and/or disgust.…”

A cortical potential reflecting cardiac function

“…Mid-and posterior insula regions appear to map physiological afferent information in an anatomically graded somatotopic mapping of the viscera (38,43,44). Rerepresentation of this afferent information by anterior insula regions is implicated as the substrate for awareness and conscious appraisal of physiological status where information about internal state is integrated with ongoing emotional processing (19,38,(40)(41)(42). Correspondingly, in patients with cardiac syndrome X, dobutamine-induced cardiac afferent sensation Association between HEPs and cardiac repolarization inhomogeneity.…”

Beyond common resources: the cortical basis for resolving task interference

“…Many previous studies have implicated these regions (particularly the DLPFC) in top-down control of processing, including the domains of selective attention (Mathalon et al, 2004;Milham et al, 2003), task-switching (Aron et al, 2004;Sussman et al, 2003), spatial attention (Giesbrecht et al, 2003;, sustained attention (Lawrence et al, 2003;Ortuno et al, 2002), emotional (Boshuisen et al, 2002;Milham et al, 2003), and autonomic control (Critchley et al, 2002(Critchley et al, , 2003. The finding that activation in this region (along with the right DLPFC) was significantly greater for No-go trials when compared to the Go trials is also consistent with the studies suggesting it monitors for response conflict Carter et al, 2001), whereby conflict signals the need for the allocation of additional control by the DLPFC (MacDonald et al, 2000).…”