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Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging

NeuroImage 17, 1384 –1393 (2002)
doi:10.1006/nimg.2002.1241
Human Vestibular Cortex as Identified with Caloric Stimulation in Functional Magnetic Resonance Imaging Oliver Fasold, Michael von Brevern, Marc Kuhberg, Christoph J. Ploner, Arno Villringer, Thomas Lempert, and Ru Department of Neurology, Charite´, Humboldt-University, D-10098 Berlin, Germany Received March 23, 2002 structures to elucidate vestibular function. Spatial ori- Anatomic and electrophysiological studies in mon-
entation and perception of movement, however, re- keys have yielded a detailed map of cortex areas re-
quire processing of vestibular information at the corti- ceiving vestibular afferents. In contrast, compara-
cal level, but comparatively little is known about the tively little is known about the cortical representation
cortical representation of the vestibular system. Ani- of the human vestibular system. In this study we ap-
mal experiments have shown that there is no primary plied caloric stimulation and fMRI to further charac-
vestibular cortex that obtains projections exclusively terize human cortical vestibular areas and to test for
from vestibular afferents (Guldin and Gru ¨ sser, 1998).
hemispheric dominance of vestibular information pro-
Instead, several multimodal sensory areas have been cessing. For caloric vestibular stimulation we used
identified, which integrate vestibular, visual, and so- cold nitrogen to avoid susceptibility artifacts induced
by water calorics. Right and left side vestibular stim-
matosensory signals (Faugier-Grimaud and Ventre, ulation was repetitively performed inducing a nystag-
1989; Fredrickson et al., 1966; Guldin and Gru mus for at least 90 s after the end of the stimulation in
1998; Odkvist et al., 1974). In humans, these areas all subjects. Only the first 60 s of this nystagmus period
have been partly confirmed by intraoperative cortical was included for statistical analysis and compared
stimulation (Foerster, 1936; Penfield, 1957), by clinical with the baseline condition. Activation maps revealed
studies in patients with acute cortical lesions (Brandt a cortical network with right hemispheric dominance,
et al., 1994), and by functional imaging using positron which in all subjects comprised the temporoparietal
emission tomography (PET) (Bottini et al., 1994). Pre- junction extending into the posterior insula and, fur-
vious imaging studies in humans provided evidence thermore, the anterior insula, pre- and postcentral
that vestibular afferents project predominantly to the gyrus, areas in the parietal lobe, the ventrolateral por-
right hemisphere but separate stimulation of both ves- tion of the occipital lobe, and the inferior frontal gyrus
tibular organs has not been performed so far to test for extending into the inferior part of the precentral sul-
this hypothesis.
cus. In conclusion, caloric stimulation in fMRI reveals
Imaging of the cortical vestibular system with func- a widespread cortical network involved in vestibular
tional magnetic resonance imaging (fMRI), the most signal processing corresponding to the findings from
useful tool in functional imaging today, has been diffi- animal experiments and previous functional imaging
cult to accomplish. Since caloric irrigation of the ears studies in humans. Furthermore, this study demon-
with hot and cold water is burdened with artifacts due strates a strong right hemispheric dominance of
vestibular cortex areas regardless of the stimulated
to the paramagnetic properties of water, some authors side, consistent with the current view of a rightward
have used galvanic (electrical) stimulation of the mas- asymmetrical cortical network for spatial orientation.
toids (Bucher et al., 1998; Lobel et al., 1998, Bense etal., 2001). Galvanic vestibular stimulation, however, 2002 Elsevier Science (USA)
differs from caloric stimulation in several aspects: 1. In previous fMRI studies, galvanic stimulation has been applied to both right and left vestibular nervessimultaneously, so that the cortical response to unilat- For a long time, vestibular research has concen- eral vestibular activation could not be studied.
trated on labyrinthine, brainstem, and cerebellar 2. Galvanic stimulation evokes primarily ocular tor- sion, wheras the induced torsional and horizontal nys- tagmus is rather weak (Zink et al., 1998) compared To whom correspondence should be addressed. Fax: ⫹ 49 (89) 2443-26014. E-mail: [email protected].
with the usual horizontal nystagmus velocity of 10 to 1053-8119/02 $35.00 2002 Elsevier Science (USA)All rights reserved.
HUMAN VESTIBULAR CORTEX 20°/s resulting from caloric stimulation; this corre- data complemented each experiment. In the first ses- sponds to a subjective illusion of tilt around the naso- sion, high-resolution 3D-Flash datasets (TR ⫽ 20 ms, occipital axis (Bense et al., 2001) during galvanic stim- TE ⫽ 5 ms, flip angle ⫽ 30°, field of view ⫽ 256 ⫻ 256 ulation, while caloric stimulation induces a constant mm, voxel size 1 ⫻ 1 ⫻ 1 mm, 190 slices) were acquired sensation of rotation.
instead of the MP RAGE to generate an individually 3. With galvanic stimulation probably all branches of reconstructed and inflated cortical surface as a detailed the vestibular nerve are activated, originating from each of the five suborgans of the laryrinth, but it iscontroversial whether galvanic stimulation affects pre- dominantly otolith afferents (Watson et al., 1998) or Caloric stimulation was applied with cold nitrogen fibers from the semicircular canals (Schneider et al., through a plastic tube into the external ear canal. The 2000). In contrast, caloric stimulation affects primarily resulting gas temperature was 5–7°C at the end of the the horizontal semicircular canal.
tube. The flow of nitrogen was adjusted to the individ- For this study, we implemented caloric vestibular ual threshold for vestibular sensations, which was activation in fMRI with gas instead of water to stimu- identified outside the scanner. Caloric nystagmus was late each vestibular organ separately. Thereby, we in- recorded once for each participant outside the scanner tended to further characterize cortical vestibular areas with horizontal electro-oculography (EOG) in complete and to test for hemispheric dominance of vestibular darkness. Nystagmus slow-phase velocities were mea- sured by hand from the graph paper by averaging 10representative slow phases during peak intensity of caloric nystagmus for each direction. Since formerstudies showed considerable interindividual variabil- ity of cortical activation (Bucher et al., 1998; Lobel etal., 1998), we performed an individual analysis of the Five individuals (four men, one woman, age range data instead of a group analysis. Each subject under- 24 –36 years) participated in the study; none had a went 6 to 10 runs comprising two caloric irrigation history of vestibular or neurological dysfunction. All cycles of 60 s each for each stimulation side. Functional subjects were right-handed according to a modified scans were acquired in complete darkness and partic- version of the Edinburgh Inventory for Handedness.
ipants had their eyes closed to prevent even minimal The study was approved by the local ethics committee.
changes of visual input during nystagmus. After the Informed consent was obtained from each participant scans, the participants were asked about their percep- prior to investigation.
tion of motion.
Data Acquisition Data Analysis Imaging was performed on a 1.5-T Siemens Vision Imaging data were analyzed using the Brainvoyager echo-planar system with a standard head coil. The 3.9 software package (R. Goebel, Max Planck Society, head was immobilized by vacuum pads to minimize Germany). The first 4 volumes of each functional run movement artifacts. Functional scans were acquired in were discarded to allow for signal equilibration, result- 16 slices covering the supratentorial parts of the brain ing in a total of 300 volumes for statistical analysis.
except for the orbitofrontal cortex in an oblique orien- The two-dimensional slice time courses were converted tation in runs of 304 images per slice using a T2*- into three-dimensional volume time courses by coreg- weighted FID echo-planar-imaging sequence (TR ⫽ 2 s, istration with the three-dimensional anatomical data TE ⫽ 60 ms, flip angle ⫽ 90°). Slice thickness was set sets from the same session and interpolation to the at 5 mm (skip 0.5 mm between slices) with 4 ⫻ 4-mm resolution of 1 mm3. Coregistration was based on the in-plane resolution (field of view ⫽ 256 ⫻ 256 mm, scanner slice position parameters for the functional imaging matrix ⫽ 64 ⫻ 64). With every functional and anatomical measurements and was visually con- session we collected a high-resolution T1-weighted trolled using the T1 scans, which were taken in the 3D-MP RAGE dataset (TR ⫽ 9.7 ms, TE ⫽ 4 ms, flip same orientation as the EPI datasets. After 3D-Motion angle ⫽ 90°, field of view ⫽ 256 ⫻ 256 mm, voxel size correction, spatially smoothing with a Gaussian kernel 1 ⫻ 1 ⫻ 1 mm, 190 slices) to transform the EPI data (FWHM ⫽ 2 mm) and linear drift removal, the statis- into three-dimensional space and to perform statistical tical maps for the individual subject were computed analysis from scans that were taken on different days with the general linear model (GLM). This required a Z (four to six sessions per subject). For visual control of transformation of the time courses prior to multiple the spatial transformation process a 2D T1-weighted regression analysis. Since motion perception can in- scan (TR ⫽ 900 ms, TE ⫽ 14 ms, voxel size 2 ⫻ 2 ⫻ 5 duce compensatory head movements only functional mm, 16 slices) in the same orientation as the functional runs that showed a displacement of less than 2 mm in FASOLD ET AL.
Cortical Areas of the Right Hemisphere Activated in Response to Unilateral Caloric Stimulation A. Parieto-insular B. Anterior insula C. Post. sup. temporal sulcus D. Post. sup. temporal gyrus E. Dorsolateral parietal area F. Inferior temporal sulcus G. Occipital lateral gyrus H. Central sulcus I. Frontoparietal operculum J. Precentral sulcus K. Dorsolateral prefrontal L. Posterior cingular sulcus M. Anterior cingular gyrus a Stimulated side.
b (⫹) refers to a BOLD signal increase in fewer than 176 neighboring interpolated voxels at our significance level of P ⬍ 10⫺9.
either direction before motion correction were in- No subject reported pain, nausea, sweating, or emo- cluded. The statistical maps were thresholded at P ⬍ tional discomfort. Corresponding to the reported self motion perception EOG recordings revealed a buildup Three dimensional cortex reconstruction was per- of nystagmus usually during the last third of the stim- formed by segmenting and tessellating the gray–white ulation period. Nystagmus lasted about 90 s with a matter boundary and by inflating (Carman et al., 1995; mean peak slow-phase velocity of 19.8°/s (SD ⫽ 5.0°/s).
Van Essen et al., 1998) the resulting surface mesh onthe basis of the Flash data. The EPI volume time BOLD Signal Increases courses of later sessions were realigned by an auto-matic intensity-based process between the 3D-MP Regardless of the stimulated side there was a strong RAGE and the 3D-Flash scan. The statistical maps for right hemispheric dominance in all subjects with re- the individual subject of all functional runs could then spect to the number of areas as well as their cluster be calculated and overlaid on the individually recon- size at the chosen statistical threshold. An exception structed surface.
was the medial surface of each hemisphere. In the To produce activation maps, baseline measurements following, clusters activated in at least one hemisphere were compared with the 60-s period after termination in at least three subjects are described. The capital of stimulus application, when the caloric nystagmus letters in parentheses in this section refer to Tables 1 peaked as confirmed by the EOG measurements out- and 2 and Figs. 1 and 2.
side the scanner. By excluding the stimulation period We found a large area of signal increase of from statistical analysis nonvestibular influences such the junction of parietal and insular cortex extending as somatosensory and auditory stimuli were mini- from the lateral sulcus into the posterior part of the mized. Between the functional runs we paused for 4 insula (A). A second significant spot of activation was min to allow the vestibular excitation to subside.
usually situated on the short gyri of the anterior insula(B). These areas could be identified in all participants (Fig. 2; Tables 1, 2).
Four main foci were ob- Motion Perception and Nystagmus served. One was found in the posterior part of the All subjects reported moderate to strong vestibular superior temporal sulcus extending into medial tempo- sensations, which they usually described as being ral gyrus in some subjects (C). Four participants had a tilted toward the nonstimulated side. Self-motion per- significant signal increase on the posterior bank of the ception started by the end of the caloric stimulation superior temporal gyrus (D), whereas the dorsolateral and in all subjects caloric stimulation led to motion parietal cortex (E) at the junction of the postcentral perception for about 90 s after the end of the stimulus.
and intraparietal sulci was activated in only three par- HUMAN VESTIBULAR CORTEX Cortical Areas of the Left Hemisphere Activated in Response to Unilateral Caloric Stimulation A. Parieto-insular B. Anterior insula C. Post. sup. temporal sulcus D. Post. sup. temporal gyrus E. Dorsolateral parietal area F. Inferior temporal sulcus G. Occipital lateral gyrus H. Central sulcus I. Frontoparietal operculum J. Precentral sulcus K. Dorsolateral prefrontal L. Posterior cingular sulcus M. Anterior cingular gyrus a Stimulated side.
b (⫹) refers to a BOLD signal increase in fewer than 176 neighboring interpolated voxels at our significance level of P ⬍ 10⫺9.
ticipants. Furthermore, four participants showed an activation focus in the inferior temporal sulcus (F).
Occipital lobe. Four participants had a significant Using caloric vestibular stimulation and susceptibil- spot of activation in the occipital cortex covering the ity-sensitive fMRI we found activation of a large-scale anterior portion of the occipital lateral gyrus (G). In the cortical network with dominance of the right hemi- fifth participant we also observed activation in this sphere, irrespective of the stimulated side. We ob-served distinct spots of activation in the parieto-insu- area, but it failed to reach the cluster size criterion of lar cortex, around the central sulcus, and in parietal, temporal, occipital, and frontal areas. In the following Central region. Cortical activations were observed we discuss how these widespread cortical activations on the pre- and postcentral gyri around the central can be interpreted with respect to vestibular cortical maps derived from animal work and previous studies Frontal lobe. In the frontal lobe we found three main foci of BOLD signal increase. One was situated inthe frontoparietal operculum of the inferior frontal gy- Temporoparietal Junction and Insula rus extending into the anterior insula in some subjects(I). Additional significant areas could be observed, in In all subjects activation could be identified at the the precentral sulcus (J) and in the dorsolateral pre- temporoparietal junction, which in some subjects ex- frontal cortex (K).
tended into the posterior insular cortex (for details onvariability of individual activations see Fig. 2). This Medial surface of the brain. Activation on the me- area corresponds closely to the parieto-insular vestib- dial surface of the brain was found in both hemispheres ular cortex (PIVC), which has been described in several in the posterior part of the cingular sulcus (L) and in monkey species (Gru ¨ sser et al., 1990; Guldin and the middle part of cingular gyrus (M). In contrast to the ¨ sser, 1998). PIVC has been postulated to be the previously described foci a consistent hemispheric core region within the vestibular cortical system with dominance could not be observed.
respect to its strong interconnections with other ves- Variability between the subjects. Individual recon- tibular cortex areas including Brodman areas 3aV, 2v, struction of the cortical surfaces revealed interindi- and 6, as well as with the vestibular nuclei in the brain vidual differences in the sulcal and gyral configuration.
stem (Guldin and Gru ¨ sser, 1998). More than 50% of Variations were also found with respect to the cluster PIVC neurons receive vestibular input (Guldin and size at the chosen statistical threshold. For illustra- ¨ sser, 1998). Other neurons of this area respond to tion, the unfolded right insular cortex is displayed sep- optokinetic or somatosensory stimuli characterizing arately for each participant in Fig. 2.
PIVC as a multimodal sensory area (Gru ¨ sser et al.,

Data of participant a are shown at a threshold of P ⬍ 10⫺9. The light and dark gray stripes symbolize the sulcal and gyral patterns of the individual unfolded hemisphere, which is shown from lateral and medial perspectives. (A) Vestibular caloric stimulation, left ear; (B)vestibular caloric stimulation, right ear. Upper row: right hemisphere; lower row: left hemisphere.

HUMAN VESTIBULAR CORTEX

FASOLD ET AL.
Spatial variation of activation in insula region. Data of the right hemisphere are shown for vestibular caloric stimulation of the left (vcl) and right (vcr) ears thresholded at P ⬍ 10⫺9. For anatomical orientation the insular sulcal pattern is stressed with a dotted line.
Anatomical landmarks: ls, lateral sulcus; stg, superior temporal gyrus; ics, insular circular sulcus; csi, central sulcus of insula.
HUMAN VESTIBULAR CORTEX 1990). Optokinetic activation of PIVC has also been subjects, we hesitate to do so with respect to the vari- shown in humans using fMRI (Dieterich et al., 1998).
ance of cortical anatomy between different species. We Brandt and colleagues (1994) demonstrated that acute think that further studies are required involving stim- lesions centered on the posterior insula cause vestibu- uli from vestibular and other sensory modalities to lar dysfunction, namely, contraversive tilting of the clarify the human functional anatomy of these presum- subjective visual vertical. Our result of PIVC activa- ably multisensory areas.
tion is further corroborated by previous imaging stud- Electrical stimulation of the superior temporal gyrus ies reporting blood flow increases in the temporopari- in awake humans causes sensations of rotation (Pen- etal junction and posterior insula as measured by PET field, 1957). Similarly, focal epileptic seizures arising during caloric stimulation (Bottini et al., 1994) and from the posterior temporal lobe may manifest with during galvanic stimulation (Bucher et al., 1998; Lobel rotational vertigo and nystagmus (Furman et al., et al., 1998, Bense et al., 2001). The interindividual 1990). An early human functional study revealed a anatomic variation of PIVC (Fig. 2) may account for the consistent focal activation in the superior temporal failure to demonstrate PIVC activation in the group region during vestibular activation (Friberg et al., analysis in some galvanic vestibular studies (Dieterich 1985). A recent galvanic study demonstrated activa- and Brandt, 2000).
tions in the superior temporal gyrus and as well in the We observed activation not only of the posterior in- middle temporal gyrus (Bense et al., 2001). Therefore, sula, but also of the anterior insula in our subjects.
we think that the temporal areas activated in our While animal studies have failed to demonstrate a study can be attributed to the human vestibular corti- vestibular input to this area, the anterior insula can be cal network.
activated by optokinetic stimulation (Dieterich et al.,1998), which interacts closely with the vestibular sys- Occipital Lobe tem. Further, a recent study investigating the human Interestingly, we observed activation ventrolaterally neural network of spatial attention demonstrated acti- in the occipital lobe in the lateral occipital gyrus. In vations bilaterally in the anterior insula (Kim et al., this location an area has been identified as the homo- 1999). The anterior insula is also known to correspond logue of monkey MT/V5 (Tootell et al., 1995; Zeki et al., to both pain and painless thermal stimuli (Davis et al., 1991). This region is now referred to as hMT/V5 ⫹ or 1998). Although our caloric stimulus was not painful MT/MST complex since it comprises also the adjacent and we excluded the stimulation period itself from area MST, which is closely linked to MT. The principal statistical analysis to avoid interference with the so- function of the MT/MST complex is visual motion de- matosensory and auditory stimulation caused by the tection and encoding of optic flow. Area MST seems to air flow, an enduring temperature stimulus can be receive also semicircular canal signals in primates assumed. Therefore, activation of the anterior insula (Bremmer et al., 1999; Thier and Erickson, 1992), cannot be reliably ascribed to vestibular mechanisms.
which may serve to compensate for head movements inthe encoding of optic flow (Andersen et al., 1999). It is unlikely that changes in retinal input caused by ves-tibular nystagmus are responsible for MT/MST activa- The visual posterior sylvian area (VPS) is situated tion in our participants, since they had their eyes posterior to PIVC in the inferior parietal lobe in the closed in darkness inside the scanner.
squirrel monkey. About 30% of the VPS neurons werefound to be vestibularly driven, while most of the neu- Central Region rons receive optokinetic or visual input (Guldin andGru ¨ sser, 1998). The neighboring area 7 also receives Activation around the central sulcus may indicate vestibular afferents (Faugier-Grimaud and Ventre, the close link of the vestibular system to the somato- 1989), but vestibularly driven units in this area were sensory system. Vestibular projections to area 3a have found to be very rare (Guldin and Gru ¨ sser, 1998). Area been found in primates. Beside vestibular-driven neu- 2v is another parietal region receiving vestibular affer- rons in the neck area of area 3a (Akbarian et al., 1994; ents and is located in the rhesus monkey at the ante- Guldin et al., 1992) vestibular input to the arm area of rior end of the intraparietal sulcus (Akbarian et al., area 3a has been described (Odkvist et al., 1974).
1994; Fredrickson et al., 1966). In humans the region Around 40% of the units in the 3a neck region are around the intraparietal sulcus is also referred to as driven by vestibular stimuli (Guldin and Gru parietal eye field and activated during eye movements 1998), and cytoarchitectonically this region may ex- (Muri et al., 1996). There is evidence that this region is tend into area 4. Compared with the circumscribed involved in spatial attention beyond the mere control of areas reported in the animal literature (Akbarian et eye movements (Kim et al., 1999). Even if it may be al., 1994; Guldin et al., 1992; Odkvist et al., 1974) the tempting to extrapolate the results from monkeys to extension of the activation spots in this region ap- activation focuses observed in the parietal lobe of our peared to be relatively large in some of our subjects.
FASOLD ET AL.
Again, an enduring temperature sensation by the ca- strong right hemispheric dominance of the activated loric stimulus, which may have contributed to this vestibular cortical network. This is consistent with the activation in the central region, cannot be excluded, current model of a distributed network for the repre- although the activations seem to be outside the so- sentation and exploration of space with hemispheric matosensory representation field of the ear canal.
dominance on the right (Mesulam, 1981, 1999). Re-cently, functional imaging revealed further experimen- Frontal Lobe Activations tal evidence for such an asymmetric large-scale neuralnetwork of spatial attention, which in many aspects Frontal activations were found in the pars opercu- overlaps with the vestibular network found in this laris of the inferior frontal gyrus extending to the in- study (Kim et al., 1999). Interestingly, vestibular stim- ferior part of the precentral sulcus. This activation ulation can transiently reverse impairment of spatial comprises Brodman area 44 and the caudal part of exploration in unilateral neglect syndrome (Cappa et Brodman area 6. Lobel et al. (1998) found activation al., 1987; Rubens, 1985). In addition to vestibular in- spots in a similar location in their study with galvanic put such a network has to integrate and process visual vestibular stimulation. Presumably these activations and somatosensory information to construct an inter- are homologous to the premotor area in monkeys, nal representation of space (Brandt and Dieterich, which is interconnected with the PIVC and VPS (Ak- barian et al., 1993, 1994). In humans an acute right- Our study has shown that caloric stimulation can be sided lesion of Brodman area 44 is known to cause successfully employed in the MRI scanner to visualize visual neglect (Husain and Kennard, 1996). Activation vestibular functions at the cortical level. This approach of the dorsolateral prefrontal cortex, which is involved may be useful for both physiological and clinical re- in eye movement control and attentional tasks (Fu- search as it combines the advantages of unilateral ves- nahashi et al., 1991) as well as in spatial attention tibular stimulation with a safe imaging procedure that (Kim et al., 1999), coincided with activation of the can be repeatedly applied. In addition, caloric stimula- frontal eye field (FEF), which is located in the vicinity tion in fMRI seems to be a particularly sensitive of the precentral sulcus and in the depth of the caudal- method for labeling of vestibular areas: this study has most part of the superior frontal sulcus (Paus, 1996).
shown significant activation of human cortex areas This activation of the FEF may be associated with that are probably homologous to the major cortical nystagmus, although a vestibular nystagmus does not areas that have been found to receive vestibular input depend on involvement of the FEF. Such activation in several primate species (Guldin and Gru ¨ sser, 1998).
either may reflect a feedback signal encoding eye posi- In addition, our approach allowed us to explore system- tion during vestibular nystagmus or, beyond mere oc- atically the laterality of the vestibular cortical net- ulomotor control, may indicate the involvement of the work, revealing a strong right hemispheric dominance.
network of spatial attention with its cortical epicenterslocated in the posterior parietal cortex, the frontal eyefields, and the cingulate gyrus (Mesulam, 1999).
Cingular Gyrus Activations Support was provided by the Deutsche Forschungsgemeinschaft (Klinische Forschergruppe der Neurologischen Klinik der Charite´ Both the anterior and posterior parts of the cingular and Grant LE 603/4-1). Oliver Fasold was supported by the graduate gyrus were activated during vestibular-stimulation. In program of the Deutsche Forschungsgemeinschaft.
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Source: http://hsinnamon.web.wesleyan.edu/wescourses/NSB-Psyc275/NeuroAnatomical%20Stories/Vestibular%20Cortex/Fasold.pdf