Attentional modulation of primary interoceptive and exteroceptive cortices

Abstract

How exteroceptive attention (EA) alters neural representations of the external world is well characterized, yet little is known about how interoceptive attention (IA) alters neural representations of the body's internal state. We contrasted visual EA against IA toward respiration. Visual EA modulated striate and extrastriate cortices and a lateral frontoparietal "executive" network. By contrast, respiratory IA modulated a posterior insula region sensitive to respiratory frequency, consistent with primary interoceptive cortex, and a posterior limbic and medial parietal network, including the hippocampus, precuneus, and midcingulate cortex. Further distinguishing between EA and IA networks, attention-dependent connectivity analyses revealed that EA enhanced visual cortex connectivity with the inferior parietal lobule and pulvinar of the thalamus, while IA enhanced insula connectivity with the posterior ventromedial thalamus, a relay of the laminar I spinothalamocortical pathway supporting interoceptive afference. Despite strong connectivity between the posterior and the anterior insula, anatomical parcellation of the insula revealed a gradient of IA to EA recruitment along its posterior-anterior axis. These results suggest that distinct networks may support EA and IA. Furthermore, the anterior insula is not an area of pure body awareness but may link representations of the outside world with the body's internal state--a potential basis for emotional experience.

Figure 1.

ROI locations along the insula cortex. ROIs were drawn to fit each visible gyrus of the template brain, yielding 8 anatomically defined regions. These regions conform to the anatomical divisions outlined in Craig (2009) and illustrated in Mesulam and Mufson (1982) and Chikama et al. (1997), representing the posterior, anterior, and accessory gyri and further subdividing these regions into dorsal and ventral subregions to capture the 3 major divisions in insular cellular layers, the granular, dysgranular, and agranular regions.

Figure 2.

Respiration signal analyses. (a) Average power and frequency of respiration as a function of attention condition, as derived from a fast Fourier transform of the respiration data across all participants. (b) Mean respiratory frequency (Hz) as a function of attention condition, as derived from a breath counting algorithm. No differentiation between attention conditions was found for respiratory rate. (c) Mean respiratory volume (arbitrary respiration belt units) as a function of attention condition, as derived from a breath counting algorithm. No differentiation between attention conditions for respiratory volume was observed. (d) Rate/volume tradeoffs for respiration as a function of attention condition. The slopes for the 2 conditions did not significantly differ. Error bars represent standard errors. Interoception plots are in dark gray and exteroception plots in light gray.

Figure 3.

Between-subject correlates of respiratory signal for IA and EA. Neural correlates of respiratory rate were modeled at the group level. (a) The most robust positive correlate of respiration during IA was found in the right posterior insula, demonstrating enhanced coupling during IA relative to EA. (b) The most robust positive correlate of respiration during EA was found in the right somatosensory cortex, demonstrating strong coupling during EA and moderate coupling during IA.

Figure 4.

Effects of attention on primary representation cortices for vision and interoception. IA recruitment (red) within the insula ROI (red border) and EA recruitment (blue) within the visual cortex ROI (blue border), as defined by the contrast between IA and EA. Peak regions in each ROI (labeled circles) were used as seeds regions to explore whole-brain functional connectivity. The breathe (red), maintain (green), suppress (blue), and baseline period (gray) % signal change plots are displayed in a bar graph for the insula and visual ROIs. Error bars represent standard errors.

Figure 5.

Insula attention tuning by anatomical partitions. A significant effect of insula location was found, such that interoceptive bias shifts to exteroceptive bias from posterior to anterior insula. All data points are presented relative to the baseline condition, as an average of left and right insula signal. (a) Right dorsal insula percent signal change plots for interoceptive and exteroceptive recruitment as a function of location. (b) Seed locations shown sagittally across the dorsal/ventral insula. (c) Right ventral insula attention tuning plots (left and right side averaged). Error bars represent standard errors. Asterisks represent areas of significant difference between IA and EA. AC = accessory gyrus; AS = anterior short gyrus; MS = middle short gyrus; PS = posterior short gyrus; AL = anterior long gyrus; PL = posterior long gyrus. Asterisks (*) denote significant (P < 0.01) IA (in red) versus EA (in blue) differences at a specific location.

Figure 6.

Whole-brain effects of attention (interoception vs. exteroception). a and b summarize the interoceptive network regions, while c and d summarize exteroceptive network regions. (a) Posterior cingulate and precuneus. (b) Hippocampus and parahippocampus. (c) Inferior parietal lobule. (d) Dorsolateral prefrontal cortex (PFC). The breathe (red), maintain (green), suppress (blue), and baseline period (gray) % signal change plots are displayed in a bar graph for each of the peak regions displayed. Error bars represent standard errors.

Figure 7.

Whole-brain functional connectivity. Whole-brain functional connectivity for the insula (A) and visual cortex (B) seeds. (C) Whole-brain PPI with the right insula interoceptive seed as a function of the IA/EA attention conditions. Right insula activity is more correlated with the thalamus during IA than EA. (d) Whole-brain PPI with the visual exteroceptive seed as a function of the attention conditions. The visual region is more correlated with the thalamus during EA than IA. The scatterplots are taken from a representative subject (whose PPI scores best matched the group PPI scores) and depict IA in red and EA in blue.