Persistence of feelings and sentience after bilateral damage of the insula

Abstract

It has been convincingly established, over the past decade, that the human insular cortices are involved in processing both body feelings (such as pain) and feelings of emotion. Recently, however, an interpretation of this finding has emerged suggesting that the insular cortices are the necessary and sufficient platform for human feelings, in effect, the sole neural source of feeling experiences. In this study, we investigate this proposal in a patient whose insular cortices were destroyed bilaterally as a result of Herpes simplex encephalitis. The fact that all aspects of feeling were intact indicates that the proposal is problematic. The signals used to assemble the neural substrates of feelings hail from different sectors of the body and are conveyed by neural and humoral pathways to complex and topographically organized nuclei of the brain stem, prior to being conveyed again to cerebral cortices in the somatosensory, insular, and cingulate regions. We suggest that the neural substrate of feeling states is to be found first subcortically and then secondarily repeated at cortical level. The subcortical level would ensure basic feeling states while the cortical level would largely relate feeling states to cognitive processes such as decision-making and imagination.

Figure 1.

(A) Three-dimensional reconstruction of patient B’s brain, using Brainvox. The right hemisphere is shown on the left (lateral view on top; mesial view below). The same 2 views of the left hemisphere are depicted on the right. The middle column shows the brain seen from the front (top) and a ventral view of the 2 hemispheres after removal of the cerebellum and brainstem (bottom). The black shaded areas reveal the extensive damage involving a large sector of both temporal lobes, the posterior aspect of the orbital frontal region, and the anterior cingulate. (See Figs 2–4 for details). (B and C) Markings of major sulci (central sulcus = red; precentral sulcus = light green; inferior frontal sulcus = yellow; horizontal branch of the Sylvian fissure = dark blue; ascending branch of the Sylvian fissure = pink; Sylvian fissure = light blue; superior temporal sulcus = dark green; anterior occipital sulcus = light brown); and positioning of coronal and axial slices as shown in Figures 2 and 3, in the brain of a normal subject, the comparison brain (B), and in Patient B. (C) The comparison brain was obtained in the same scanner used for Patient B.

Figure 2.

Coronal slices through the comparison brain and through patient B’s brain. The images are presented in radiological convention (right is on left and left is on right). The orientation and level of the slices in the comparison brain were matched to those in patient B. (see Fig. 1B,C). The first, third, and fifth rows (I, III, and V) show slices of the comparison brain; the second, fourth, and sixth (II, IV, and VI) those of patient B. The relevant sulci marked on the 3D reconstructed brains (see Fig. 1B,C) were automatically transferred to each slice that intersects them using Brainvox. The lesion seen in Patient B was manually transferred onto each corresponding slice of the comparison brain (areas in light brown), using the marked sulci as reference. Slice setting as seen in Figure 1. The coronal slices reveal complete damage of the insula, from its anterior-most edge (panel 4, row I and II) to its most posterior (panel 1, row V and VI), highlighted within the red ovals (continuous line for the comparison brain; dashed line for Patient B’s brain). The damage involves all tissue between the lateral insula surface and the outer limit of the lenticular nucleus destroying all insular cortex, extreme capsule, claustrum, and external capsule. The damage continues without interruption into the orbital sector adjacent to the insula (panels 4 and 5 in row I and II, and panels 1 and 2 in row III and IV), highlighted by blue ovals and circles. For additional detail of posterior orbito-frontal damage, see Figure 4. The lesion extends into both temporal lobes where it destroys the polar region (panels 3 and 4 in rows I and II), the amygdalae (panels 2 and 3 in rows III and IV), the hippocampuses and the parahippocampal gyri (panels 3 and 4 in rows III and IV and panel 5 and panels 1, 2, and 3 in rows V and VI). In the right hemisphere, the damage extends further posteriorly in the dorsolateral and inferior aspects of the temporal lobes. There is also partial damage to the frontoparietal operculum (panels 1–3 in rows III and IV). The brainstem is intact (see panel 5 in rows III and IV and panels 1 and 2 in rows V and VI; the brainstem is highlighted in continuous yellow circles); the cerebellum is also intact.

Figure 3.

Axial slices of the comparison brain and of patient B’s brain, interleaved as in Figure 2. The comparison brain shows the transfer of the area damaged in Patient B. Slice setting as in Figure 1B,C. There is again evidence of the complete damage of the insula, the underlying white matter and the claustrum in both hemispheres, highlighted by the red ovals. See panels 1–3 in rows III and IV. The damage also encompasses both temporal lobes destroying the polar regions, the amygdalae, the hippocampuses, and the parahippocampal gyri (panels 3–5 in rows I and II). In the right hemisphere, the damage extends further posteriorly in the inferior and mesial aspects. The damage involves the posterior fronto-orbital region bilaterally (highlighted by the blue circles in panel 5, rows I and II); the damage extends dorsally to involve the anterior cingulate cortex subcalosally and beyond (panel 1 in rows III and IV), and the white matter in the core of both frontal lobes more extensively in the right hemisphere (all panels in rows III and IV). The brainstem and cerebellum are intact (see panels 1–5 in rows I and II; brainstem circled in yellow), as are all sensory and motor cortices, and the association cortices of the parietal and occipital lobes, and the primary visual regions.

Figure 4.

Detail of the posterior orbital sector, basal forebrain region, and basal ganglia in the comparison brain and in patient B. The yellow colored slabs in the right lower corner represent the section of brain from which the panels of this figure were extracted. The slices in patient B. are 1.5-mm thick, and all consecutive cuts are shown. The slices in the comparison brain are anatomically matched to those of patient B. Rows of panels from the comparison brain are interleaved with those from Patient B., as in the previous figures. Several structures are colored. The same color is used for the comparison brain and Patient B’s brain. In Patient B., the dorsal striatum (putamen and caudate nuclei, in blue) appears intact. The ventral striatum/nucleus accumbens region (red), largely located below and in front of the anterior commissure is also seen in patient B. The whole basal ganglia complex appears to be diminished in size; partial damage is possible (see text). The basal forebrain nuclear masses (septal nuclei; diagonal band; substantia innominate), shown in greenish yellow in the comparison brain, are missing in Patient B. The posterior orbitofrontal cortices (green) and the claustrum (pink) are also missing in Patient B.

Figure 5.

(A) Right and left hemispheres of the comparison brain seen in lateral views with the postcentral gyrus (SI) shown in green. In the center, a view of the brain’s undersurface after the temporal lobes were removed to allow inspection of the lower surface of the fronto-parietal opercula. SII is shown in light blue. (B) Same as in A for the brain of Patient B. Both SI and SII areas are intact.