Identifying human parieto-insular vestibular cortex using fMRI and cytoarchitectonic mapping

Abstract

The parieto-insular vestibular cortex (PIVC) plays a central role in the cortical vestibular network. Although this region was first defined and subsequently extensively studied in nonhuman primates, there is also ample evidence for a human analogue in the posterior parietal operculum. In this study, we functionally and anatomically characterize the putative human equivalent to macaque area PIVC by combining functional magnetic resonance imaging (fMRI) of the cortical response to galvanic vestibular stimulation (GVS) with probabilistic cytoarchitectonic maps of the human parietal operculum. Our fMRI data revealed a bilateral cortical response to GVS in posterior parieto-insular cortex. Based on the topographic similarity of these activations to primate area PIVC, we suggest that they constitute the functionally defined human equivalent to macaque area PIVC. The locations of these activations were then compared to the probabilistic cytoarchitectonic maps of the parietal operculum (Eickhoff et al. [2005a]: Cereb Cortex, in press; Eickhoff et al. [2005c]: Cereb Cortex, in press), whereby the functionally defined PIVC matched most closely the cytoarchitectonically defined area OP 2. This activation of OP 2 by vestibular stimulation and its cytoarchitectonic features, which are similar to other primary sensory areas, suggest that area OP 2 constitutes the human equivalent of macaque area PIVC.

Figure 1

Schematic drawing of the monkey brain, showing the location of vestibular areas in nonhuman primates. The areas that have been shown to receive vestibular input are area 2v at the tip of the intraparietal sulcus, area 3av in the central sulcus (i.e., the neck representation in somatosensory area 3a), areas 7a and 7b in the inferior parietal lobe, precentral area 6, and the parieto‐insular vestibular cortex (PIVC) in the posterior parietal operculum in the depth of the Sylvian fissure.

Figure 2

The cytoarchitectonic organization of the human parietal operculum, shown as a maximum probability map (MPM) projected onto a surface rendering of the Montreal Neurological Institute (MNI) single‐subject template. The temporal lobes were removed for display purposes. Four distinct architectonic areas can be identified in this region: OP 1–4 [Eickhoff et al.,2005c].

Figure 3

Left panel: Relative increases in blood oxygenation level‐dependent (BOLD) signal (for the 11 subjects) associated with the excitation of the right and inhibition of the left vestibular nerve (i.e., left anodal to right cathodal galvanic vestibular stimulation, condition LR) relative to rest. Areas of significant relative increase in BOLD signal (P < 0.00005, uncorrected) are shown superimposed on a surface‐rendered Montreal Neurological Institute (MNI) single‐subject template to detail the macroanatomic location of the activations. The exact coordinates and the height of the local maxima within the areas of activation as well as quantitative descriptions (probabilities) of their cytoarchitectonic assignments are given in Table I. The green numbers in the figure point to the respective cluster label in Table I. Right panel: Orthogonal sections at × = 38, y = −26, z = 20, i.e., the location of the local maximum of the cluster centered upon the right posterior parietal operculum (Cluster 1) corresponding to parieto‐insular vestibular cortex (PIVC). The extent of OP 1 (white), OP 2 (dark gray), OP 3 (light gray), and OP 4 (intermediate gray) is shown in different gray values superimposed on the MNI single‐subject template.

Figure 4

Left panel: The regions where there is a significant relative blood oxygenation level‐dependent (BOLD) signal increase associated with the excitation of the left and inhibition of the right vestibular nerve (i.e., right anodal to left cathodal galvanic vestibular stimulation, condition RL) relative to rest. Areas of significant relative increase in BOLD signal (P < 0.00005, uncorrected) are shown superimposed on a surface‐rendered Montreal Neurological Institute (MNI) single‐subject template to detail the macroanatomy. The height and the exact coordinates of the local maxima within the areas of activation as well as quantitative descriptions of their cytoarchitectonic assignments are given in Table I. The green numbers in the figure point to the respective cluster label in this table. Middle panel: Detailed view on orthogonal sections at x = −38, y = −22, z = 20, i.e., the location of the local maximum of the cluster centered upon the left posterior parietal operculum (Cluster 1) corresponding to parieto‐insular vestibular cortex (PIVC). The extent of OP 1 (white), OP 2 (dark gray), OP 3 (light gray), and OP 4 (intermediate gray) is shown in different gray values; the MNI single‐subject template is shown in the background. Right panel: Detail views focused on the location of the local maximum in the right posterior parietal operculum (Cluster 2, x = 40, y = −26, z = 22)

Figure 5

A: Synopsis of the significant activations for both stimulation modes. Activations in condition RL are shown in green, those in condition LR in red. The two patterns of activation only overlap in a small region in the right hemisphere. B: Results of the conjunction analysis. The displayed region was significantly activated in both stimulation conditions and is associated significantly with the main effect of galvanic vestibular stimulation (irrespective of anode side) relative to rest. C: Orthogonal sections through the location of the local maximum revealed by the conjunction analysis, which was located in the right posterior parietal operculum (Cluster 1, x = +38, y = −26, z = +22).

Figure 6

The blood oxygenation level‐dependent (BOLD) signal changes (in percent) per condition are displayed for OP 2 in both hemispheres. The values shown are the mean (± SEM) percent signal changes for the voxel within OP 2 in each subject, which was associated most strongly with the main effect of galvanic vestibular stimulation. That there is a considerable degree of lateralization into the right hemisphere for the response to contralateral stimulation, i.e., the response of right area OP 2 to excitation of the left vestibular nerve was considerably stronger than was the BOLD signal change in OP 2 of the left hemisphere caused by stimulation of the right vestibular nerve.

Figure 7

Comparison between the location of secondary somatosensory cortex (SII) as revealed by a meta‐analysis of 181 functional imaging activations [Eickhoff et al.,2005a] shown in yellow and the location of parieto‐insular vestibular cortex (PIVC) identified by the conjunction analysis reported in this study, shown in red. The temporal lobes were removed for display purposes (cf. Fig. 2). Significant clusters are clearly separated from each other and are also located in different cytoarchitectonic areas: Whereas the location of SII corresponds mainly to OP 1 and OP 4, PIVC is located in area OP 2.

Figure 8

A) Microphotograph of area OP 2 from a cell body‐stained histological section. The thin cortex of OP 2 shows small infragranular layers, a sharply defined white matter border, and a distinct horizontal lamination. Prominent pyramidal cells in layer III are rare. The cytoarchitecture of OP 2 is more similar to that of Brodmann area (BA) 3b (B), i.e., the primary somatosensory cortex, than to the unimodal somatosensory association area BA 1 (C). Roman numbers designate cortical layers.