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Neuroanatomical substrates for the volitional regulation of heart rate.

Jones CL, Minati L, Nagai Y, Medford N, Harrison NA, Gray M, Ward J, Critchley HD - Front Psychol (2015)

Bottom Line: In contrast, activation of ventrolateral prefrontal and parietal cortices occurred when attempting to decrease heart rate.Biofeedback enhanced activity within occipito-temporal cortices, but there was no significant interaction with task conditions.Activity in regions including pregenual anterior cingulate and ventral striatum reflected the magnitude of successful task performance, which was negatively related to subclinical anxiety symptoms.

View Article: PubMed Central - PubMed

Affiliation: Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex Brighton, UK ; Department of Psychiatry and Sackler Centre for Consciousness Science, Clinical Imaging Sciences Centre, University of Sussex Brighton, UK.

ABSTRACT
The control of physiological arousal can assist in the regulation of emotional state. A subset cortical and subcortical brain regions are implicated in autonomic control of bodily arousal during emotional behaviors. Here, we combined human functional neuroimaging with autonomic monitoring to identify neural mechanisms that support the volitional regulation of heart rate, a process that may be assisted by visual feedback. During functional magnetic resonance imaging (fMRI), 15 healthy adults performed an experimental task in which they were prompted voluntarily to increase or decrease cardiovascular arousal (heart rate) during true, false, or absent visual feedback. Participants achieved appropriate changes in heart rate, without significant modulation of respiratory rate, and were overall not influenced by the presence of visual feedback. Increased activity in right amygdala, striatum and brainstem occurred when participants attempted to increase heart rate. In contrast, activation of ventrolateral prefrontal and parietal cortices occurred when attempting to decrease heart rate. Biofeedback enhanced activity within occipito-temporal cortices, but there was no significant interaction with task conditions. Activity in regions including pregenual anterior cingulate and ventral striatum reflected the magnitude of successful task performance, which was negatively related to subclinical anxiety symptoms. Measured changes in respiration correlated with posterior insula activation and heart rate, at a more lenient threshold, change correlated with insula, caudate, and midbrain activity. Our findings highlight a set of brain regions, notably ventrolateral prefrontal cortex, supporting volitional control of cardiovascular arousal. These data are relevant to understanding neural substrates supporting interaction between intentional and interoceptive states related to anxiety, with implications for biofeedback interventions, e.g., real-time fMRI, that target emotional regulation.

No MeSH data available.


Related in: MedlinePlus

Visual display of feedback ‘thermometer.’ There were six task conditions within the experiment which embodied a 2 × 3 factorial design. The factors were (1) the direction of intended heart rate change (increase = ‘arousal’/and decrease = ‘relaxation’) and (2) the presence and veracity of visual feedback (true feedback accurately reflecting heart rate; false feedback, i.e., random fluctuation and absent feedback). Each condition was performed twice by the participant and presented in pseudorandom sequences that avoided immediate repetition of the same task condition. Participants were instructed to use arousal to make the thermometer level rise in the increased heart rate conditions and relaxation in the lower in the heart rate conditions. Below are tabulated the biofeedback task conditions undertaken during the course of the experiment.
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Figure 1: Visual display of feedback ‘thermometer.’ There were six task conditions within the experiment which embodied a 2 × 3 factorial design. The factors were (1) the direction of intended heart rate change (increase = ‘arousal’/and decrease = ‘relaxation’) and (2) the presence and veracity of visual feedback (true feedback accurately reflecting heart rate; false feedback, i.e., random fluctuation and absent feedback). Each condition was performed twice by the participant and presented in pseudorandom sequences that avoided immediate repetition of the same task condition. Participants were instructed to use arousal to make the thermometer level rise in the increased heart rate conditions and relaxation in the lower in the heart rate conditions. Below are tabulated the biofeedback task conditions undertaken during the course of the experiment.

Mentions: Heart rate and breathing rate were monitored continuously throughout the tasks. The biofeedback signal of physiological relaxation and arousal was represented by a visible thermometer with a blue bar that reflected heart rate (Figure 1). The starting point (near top or bottom) and approximate sensitivity was tailored for each participant by task condition. In the relaxation conditions, participants were instructed by a cue to try to make the bar go down by physiologically relaxing, conversely in the arousal task participants were instructed to make the bar rise by becoming more physiologically aroused. Thus the nebulous terms relaxation and arousal were operationalized, as in previous studies, to refer to heart rate decreases and increases, respectively. In the false feedback condition, the bar fluctuated following a smooth random walk. In the no-feedback condition there was no bar, with only the outline of a thermometer displayed. All participants knew that the purpose of the study was to control their own heart rate. Participants were informed that the thermometer reflected their heart rate, where a rise in heart rate was displayed as a rise in the level depicted on the thermometer which signaled an increase in physiological arousal. Similarly, participants were told that a drop in heart rate was displayed as a lowering of the level depicted on the thermometer which in turn signaled a reduction in physiological arousal, which we termed ‘relaxation.’ They were advised (when possible) to use the feedback and were also told that, during scanning, the feedback would be altered or removed for some trials, which might make it harder for them to achieve the required increase or decrease in arousal/heart rate. Practice trials were performed before scanning, in which participants were given only true heart rate feedback and were instructed to make to bar go down by relaxing and to make the bar rise by increasing the level of arousal, operationalized to mean heart rate, and reinforced by this practice session. These instructions were carried over to their performance within the scanner. Here again, the instruction to volitionally increase heart rate was displayed by the visual cue ‘AROUSAL’ and the instruction to volitionally decrease heart rate was displayed by the visual cue ‘RELAXATION’ at the start of each 90 s block (replacing the text shown in the upper part of Figure 1). The false feedback conditions were not explicitly distinguished from the true feedback conditions.


Neuroanatomical substrates for the volitional regulation of heart rate.

Jones CL, Minati L, Nagai Y, Medford N, Harrison NA, Gray M, Ward J, Critchley HD - Front Psychol (2015)

Visual display of feedback ‘thermometer.’ There were six task conditions within the experiment which embodied a 2 × 3 factorial design. The factors were (1) the direction of intended heart rate change (increase = ‘arousal’/and decrease = ‘relaxation’) and (2) the presence and veracity of visual feedback (true feedback accurately reflecting heart rate; false feedback, i.e., random fluctuation and absent feedback). Each condition was performed twice by the participant and presented in pseudorandom sequences that avoided immediate repetition of the same task condition. Participants were instructed to use arousal to make the thermometer level rise in the increased heart rate conditions and relaxation in the lower in the heart rate conditions. Below are tabulated the biofeedback task conditions undertaken during the course of the experiment.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4373272&req=5

Figure 1: Visual display of feedback ‘thermometer.’ There were six task conditions within the experiment which embodied a 2 × 3 factorial design. The factors were (1) the direction of intended heart rate change (increase = ‘arousal’/and decrease = ‘relaxation’) and (2) the presence and veracity of visual feedback (true feedback accurately reflecting heart rate; false feedback, i.e., random fluctuation and absent feedback). Each condition was performed twice by the participant and presented in pseudorandom sequences that avoided immediate repetition of the same task condition. Participants were instructed to use arousal to make the thermometer level rise in the increased heart rate conditions and relaxation in the lower in the heart rate conditions. Below are tabulated the biofeedback task conditions undertaken during the course of the experiment.
Mentions: Heart rate and breathing rate were monitored continuously throughout the tasks. The biofeedback signal of physiological relaxation and arousal was represented by a visible thermometer with a blue bar that reflected heart rate (Figure 1). The starting point (near top or bottom) and approximate sensitivity was tailored for each participant by task condition. In the relaxation conditions, participants were instructed by a cue to try to make the bar go down by physiologically relaxing, conversely in the arousal task participants were instructed to make the bar rise by becoming more physiologically aroused. Thus the nebulous terms relaxation and arousal were operationalized, as in previous studies, to refer to heart rate decreases and increases, respectively. In the false feedback condition, the bar fluctuated following a smooth random walk. In the no-feedback condition there was no bar, with only the outline of a thermometer displayed. All participants knew that the purpose of the study was to control their own heart rate. Participants were informed that the thermometer reflected their heart rate, where a rise in heart rate was displayed as a rise in the level depicted on the thermometer which signaled an increase in physiological arousal. Similarly, participants were told that a drop in heart rate was displayed as a lowering of the level depicted on the thermometer which in turn signaled a reduction in physiological arousal, which we termed ‘relaxation.’ They were advised (when possible) to use the feedback and were also told that, during scanning, the feedback would be altered or removed for some trials, which might make it harder for them to achieve the required increase or decrease in arousal/heart rate. Practice trials were performed before scanning, in which participants were given only true heart rate feedback and were instructed to make to bar go down by relaxing and to make the bar rise by increasing the level of arousal, operationalized to mean heart rate, and reinforced by this practice session. These instructions were carried over to their performance within the scanner. Here again, the instruction to volitionally increase heart rate was displayed by the visual cue ‘AROUSAL’ and the instruction to volitionally decrease heart rate was displayed by the visual cue ‘RELAXATION’ at the start of each 90 s block (replacing the text shown in the upper part of Figure 1). The false feedback conditions were not explicitly distinguished from the true feedback conditions.

Bottom Line: In contrast, activation of ventrolateral prefrontal and parietal cortices occurred when attempting to decrease heart rate.Biofeedback enhanced activity within occipito-temporal cortices, but there was no significant interaction with task conditions.Activity in regions including pregenual anterior cingulate and ventral striatum reflected the magnitude of successful task performance, which was negatively related to subclinical anxiety symptoms.

View Article: PubMed Central - PubMed

Affiliation: Clinical Imaging Sciences Centre, Brighton and Sussex Medical School, University of Sussex Brighton, UK ; Department of Psychiatry and Sackler Centre for Consciousness Science, Clinical Imaging Sciences Centre, University of Sussex Brighton, UK.

ABSTRACT
The control of physiological arousal can assist in the regulation of emotional state. A subset cortical and subcortical brain regions are implicated in autonomic control of bodily arousal during emotional behaviors. Here, we combined human functional neuroimaging with autonomic monitoring to identify neural mechanisms that support the volitional regulation of heart rate, a process that may be assisted by visual feedback. During functional magnetic resonance imaging (fMRI), 15 healthy adults performed an experimental task in which they were prompted voluntarily to increase or decrease cardiovascular arousal (heart rate) during true, false, or absent visual feedback. Participants achieved appropriate changes in heart rate, without significant modulation of respiratory rate, and were overall not influenced by the presence of visual feedback. Increased activity in right amygdala, striatum and brainstem occurred when participants attempted to increase heart rate. In contrast, activation of ventrolateral prefrontal and parietal cortices occurred when attempting to decrease heart rate. Biofeedback enhanced activity within occipito-temporal cortices, but there was no significant interaction with task conditions. Activity in regions including pregenual anterior cingulate and ventral striatum reflected the magnitude of successful task performance, which was negatively related to subclinical anxiety symptoms. Measured changes in respiration correlated with posterior insula activation and heart rate, at a more lenient threshold, change correlated with insula, caudate, and midbrain activity. Our findings highlight a set of brain regions, notably ventrolateral prefrontal cortex, supporting volitional control of cardiovascular arousal. These data are relevant to understanding neural substrates supporting interaction between intentional and interoceptive states related to anxiety, with implications for biofeedback interventions, e.g., real-time fMRI, that target emotional regulation.

No MeSH data available.


Related in: MedlinePlus