Differential responses of the insular cortex gyri to autonomic challenges

Abstract

Determining insular functional topography is essential for assessing autonomic consequences of neural injury. We examined that topography in the five major insular cortex gyri to three autonomic challenges, the Valsalva, hand grip, and foot cold pressor, using functional magnetic resonance imaging (fMRI) procedures. Fifty-seven healthy subjects (age ± std: 47 ± 9 years) performed four 18 s Valsalva maneuvers (30 mm Hg load pressure), four hand grip challenges (16 s at 80% effort), and a foot cold pressor (60 s, 4°C), with fMRI scans recorded every 2 s. Signal trends were compared across gyri using repeated measures ANOVA. Significantly (P<0.05) higher signals in left anterior versus posterior gyri appeared during Valsalva strain, and in the first 4 s of recovery. The right anterior gyri showed sustained higher signals up to 2 s post-challenge, relative to posterior gyri, with sub-gyral differentiation. Left anterior gyri signals were higher than posterior areas during the hand grip challenge. All right anterior gyri showed increased signals over posterior up to 12 s post-challenge, with decline in the most-anterior gyrus from 10 to 24 s during recovery. The left three anterior gyri showed relatively lower signals only during the 90 s recovery of the cold pressor, while the two most-anterior right gyri signals increased only during the stimulus. More-differentiated representation of autonomic signals appear in the anterior right insula for the Valsalva maneuver, a bilateral, more-posterior signal representation for hand grip, and preferentially right-sided, anterior-posterior representation for the cold pressor. The functional organization of the insular cortex is gyri-specific to unique autonomic challenges.

Copyright © 2012. Published by Elsevier B.V.

Figures

Figure 1. Subregions of the anterior and posterior insular cortex

The PLG, ALG, PSG, MSG, and ASG are shown overlaid on the average of 57 healthy control subjects’ anatomical scans (normalized to MNI space, left side, sagittal slice at −38 mm).

Figure 2. Physiologic responses to autonomic challenges

Heart rate responses to the autonomic challenges are shown across the series and averaged over repeated challenges (Valsalva and hand grip) with time-points of significance response from baseline denoted above the right-hand traces (RMANOVA, P

Figure 3. fMRI signal responses across insular cortex gyri, averaged over four 18-second Valsalva maneuvers in 57 subjects

The top graphs illustrate signal differences between gyri, relative to the PLG. The middle section illustrates time-points of statistically significant differences between gyri (P

Figure 4. fMRI signal responses across insular cortex gyri, averaged over four 16-second hand grip challenges in 57 subjects

The top graphs illustrate signal difference between gyri, relative to the PLG. The middle section illustrates time-points of statistically significant difference between gyri (P

Figure 5. fMRI signal responses across insular cortex gyri, averaged over one 60 second cold pressor challenge in 57 subjects

The top graphs illustrate signal difference between gyri, relative to the PLG. The middle section illustrates time-points of statistically significant difference between gyri (P

Figure 6. Lateralization of Valsalva BOLD responses

The fMRI BOLD responses (mean ± SE, N = 57) to the Valsalva are shown on the right relative to the left side for each gyri, with all right gyri showing predominantly higher signals on the right over the left (P