How the heart speaks to the brain: neural activity during cardiorespiratory interoceptive stimulation - PubMed (original) (raw)

How the heart speaks to the brain: neural activity during cardiorespiratory interoceptive stimulation

Mahlega S Hassanpour et al. Philos Trans R Soc Lond B Biol Sci. 2016.

Abstract

Prominent theories emphasize key roles for the insular cortex in the central representation of interoceptive sensations, but how this brain region responds dynamically to changes in interoceptive state remains incompletely understood. Here, we systematically modulated cardiorespiratory sensations in humans using bolus infusions of isoproterenol, a rapidly acting peripheral beta-adrenergic agonist similar to adrenaline. To identify central neural processes underlying these parametrically modulated interoceptive states, we used pharmacological functional magnetic resonance imaging (phMRI) to simultaneously measure blood-oxygenation-level dependent (BOLD) and arterial spin labelling (ASL) signals in healthy participants. Isoproterenol infusions induced dose-dependent increases in heart rate and cardiorespiratory interoception, with all participants endorsing increased sensations at the highest dose. These reports were accompanied by increased BOLD and ASL activation of the right insular cortex at the highest dose. Different responses across insula subregions were also observed. During anticipation, insula activation increased in more anterior regions. During stimulation, activation increased in the mid-dorsal and posterior insula on the right, but decreased in the same regions on the left. This study demonstrates the feasibility of phMRI for assessing brain activation during adrenergic interoceptive stimulation, and provides further evidence supporting a dynamic role for the insula in representing changes in cardiorespiratory states.This article is part of the themed issue 'Interoception beyond homeostasis: affect, cognition and mental health'.

Keywords: cardiac; emotion; insula; interoception; pharmacological functional magnetic resonance imaging; respiration.

© 2016 The Author(s).

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Figures

Figure 1.

Figure 1.

(a) Experimental design for the concurrent BOLD/ASL isoproterenol infusion study. (b) Mean heart rate changes during the saline, 0.25, 1 and 2 mcg infusion scans. (c) Interoceptive detection rates for each infusion. (d) Body map showing the proportional location of heartbeat sensations across study participants at 2 mcg. The chest showed the greatest overlap.

Figure 2.

Figure 2.

(a) Voxelwise whole brain analysis reveals activation of the right mid-dorsal and posterior insula during cardiorespiratory stimulation with isoproterenol at 2 mcg (peak versus baseline; p < 0.05, corrected). Insula activation is shown in coronal, axial and sagittal views. (b) Differing patterns of BOLD and ASL signals were observed in this region during different doses. For BOLD, we observed dose-dependent increases, whereas for ASL the increase was only observed at 2 mcg.

Figure 3.

Figure 3.

Cortical activity during the anticipatory period immediately after infusion administration, prior to onset of heart rate changes. Activation was observed in the right mid-dorsal and anterior insula, right postcentral gyrus and precuneus (voxelwise whole brain analysis, thresholded at p < 0.001, uncorrected). D, dorsal; V, ventral; L, left; R, right. Numbers indicate MNI coordinates for each axial slice.

Figure 4.

Figure 4.

Time series showing the BOLD signal over time in the left and right insula following infusion onset. Middle panels: right insula clusters passing the significance threshold during the anticipatory period (red), peak period (green) and their overlap (yellow). For comparison, contralateral regions in the left insula are shown. The time course of BOLD signal change averaged across all 21 subjects is displayed for each set of clusters during the saline (left panel) and 2 mcg (right panel) infusions. This figure suggests the presence of different response patterns for the left and right insula subregions, with (i) increased anterior responses during anticipation, (ii) increased mid-dorsal and posterior responses on the right during stimulation and (iii) decreased mid-dorsal and posterior responses on the left during stimulation. Since the first 4 volumes were discarded to allow the MR signals to reach steady-state, the plots show BOLD activity from 14 to 240 s.

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