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A number of behavioral and neuroimaging studies have reported converging data in favor of a cortical network for vestibular function, distributed between the temporo-parietal cortex and the prefrontal cortex in the primate. In this review, we focus on the role of the cerebral cortex in visuo-vestibular integration including the motion sensitive temporo-occipital areas i.
Indeed, these two neighboring cortical regions, though they both receive combined vestibular and visual information, have distinct implications in vestibular function. In sum, this review of the literature leads to the idea of two separate cortical vestibular sub-systems forming 1 a velocity pathway including MST and direct descending pathways on vestibular nuclei.
This vestibular cortical pathway would be implicated in high-order multimodal integration and cognitive functions, including world space and self-referential processing.
Since the early clinical observations suggestive of a cortical role in vestibular function Carmichael et al. Thus, by neural unit recordings, discharges of neurons located in the visual associative cortex were observed during body rotations in cat Becker et al. More precisely, visual tracking neurons were found in monkey to receive vestibular information in cortical sites located in the associative parietal and temporal cortex Kawano et al.
In our early work studying effects of cortical lesions in the cat Ventre, a , b , we described a parcellation of visuo-vestibular areas distributed in the suprasylvian SS cortex divided into two regions: the middle SS gyrus area 7 preferentially involved in vestibularly driven ocular responses and the lateral SS sulcus implicated in optokinetic ocular responses.
Similarly, a pattern of visual extrastriate areas localized in the superior temporal sulcus in monkey and described as MT middle temporal and MST middle superior temporal areas were found to be activated during visual motion as well as during visuo-vestibular interactions Komatsu and Wurtz, a , b ; Newsome et al. Indeed, based on recent data on neuronal receptive field properties and visual behavior Lomber and Payne, , this lateral suprasylvian sulcus area PMLS is equated to the visual areas located in the middle temporal sulcus in macaque monkey.
By combining lesions and tracer injections Ventre and Faugier-Grimaud, , ; Faugier-Grimaud and Ventre, or electrophysiology and tracer injections Akbarian et al. Only recently, over the last two decades, the advanced neuroimaging techniques have given access to the investigation of human brain activation elicited during either caloric ear irrigation or galvanic vestibular stimulation Bottini et al.
These authors demonstrated in healthy subjects that such vestibular stimulations triggered activity in distributed cortical areas including the posterior temporo-parietal and retro-insular cortex, the intraparietal sulcus homologue to area 2v , the somatosensory area 3 as well as rostrally several frontal regions middle and inferior frontal gyri and the anterior cingulate cortex. Interestingly, there is a striking homology between the vestibular cortical networks described in monkey and in man see for review, Fukushima, ; Brandt and Dieterich, ; Lopez and Blanke, Figure 1 illustrates the inter-species organization and growing complexity of the vestibular cortical fields.
While convincing evidence is now provided for a link between vestibular function and cortical processes, the exact roles of these various cortical sites topographically similar in animal and human, remain obscure. Recent studies suggest a role of some of these cortical vestibular sites in cognitive processes relying on vestibular integration i. Schematic brain representations illustrating the topography of the vestibular cortical fields as they have been experimentally identified in cat, monkey, and human.
In the right panel are listed the vestibular sites with their localization in the cortical regions. In cat: the marginal sulcus mars , the anterior ass , middle mss and posterior pss suprasylvian sulci, the anterior aes and posterior pes ectosylvian sulci. On the basis of the subcortical organization of the vestibular function largely described in the past Robinson, ; Raphan et al. Such a dual path organization of the vestibular system is also reflected in vestibular evoked control of goal-directed arm movements Bresciani et al.
In the following review of the literature, we will attempt to draw a parallel between such a dual organization of the vestibular function as demonstrated in subcortical regions, and the organization of the temporo- parietal cortex. Thus, we hypothesize that the cortical integration of vestibular information is organized as a twofold system of pathways originating from the temporal and parietal cortices which respectively mediate vestibularly driven velocity and inertial signals.
As the cortical properties have been extensively investigated in human and non-human primate, we will mainly refer in the following to the studies describing the cortical processes linked to ego-motion in these species. However, the inter-species similarities described above demonstrate the functional coherence and evolutionary continuity that emphasize the physiological foundations for visual and vestibular interactions in the cerebral cortex especially in the parietal and temporal lobes.
In order to differentiate between the motion of the visual surrounding versus self-motion, the central nervous system must integrate multimodal signals including visual and vestibular signals in order to extract the origin and direction of the perceived movement.
As mentioned above, cortical visual and vestibular interaction has been first suggested in the visual lateral suprasylvian cortex in cat Vanni-Mercier and Magnin, a , b ; Ventre, a , b ; Rauschecker et al. These visual temporal cortical areas called MT middle temporal and MST middle superior temporal have a critical role in visual motion processes linked to smooth pursuit, heading perception and optokinetic-related information, all involving velocity signals triggered during ego-motion in monkey.
In the following, we will see how the visual and vestibular signals are processed in the temporal cortex MST to provide velocity information about ego-motion. The main findings leading to the idea of a velocity pathway in the temporal cortical region will be developed in the two next sections successively for the integration of visual visual motion and vestibular body motion kinetic inputs.
Their majority of cells responsive to moving visual stimuli is linked to smooth pursuit SP in a preferred direction but differed in the size of their receptive fields, with MST having larger receptive fields Zeki, ; Komatsu and Wurtz, a , b , These extrastriate visual areas have been first described for their role in pursuit and compensatory eye movement generation due to visual field displacements and more recently they have been implicated in self-motion and heading perception.
In the context of self-motion, the most interesting units are in MST, the pursuit cells preferentially activated during moving background Erickson and Dow, ; Inaba et al.
Such pursuit cells have opposite preferred direction for pursuit and visual motion leading to a synergistic response during pursuit in the light Erickson and Dow, Interestingly as suggested by Komatsu and Wurtz b , such a synergistic response of MST neurons might be to increase the pursuit response of these cells to compensate for the optokinetic nystagmus.
Even though suggested by these electrophysiological works in monkey, the idea of a role of MST in visuo-vestibular function in the primate will only clearly emerge from focal lesions studies. Thus, Dursteler and Wurtz demonstrated that chemical lesions in MST can induce twofold deficits in optokinetic nystagmus OKN 1 a reduction in the slow OKN build-up related to a directional pursuit deficit toward the lesioned side and 2 a reduction in the fast OKN build-up related to a retinal deficit with no specific directional preponderance.
In accordance with our own observations in the cat Ventre, a , b , these findings were the first demonstration in monkey of the contribution of extrastriate cortex, including MST on OKN generation.
In humans, OKN deficits described with a reduction of ipsiversive slow phase velocity have been reported first in large cortical lesions, including parietal cortex Carmichael et al. Taken together, these observations argue in favor of a role of MST area in computation of velocity signals issued from moving surrounding objects and used to produce pursuit and compensatory eye movements like OKN. This MST activity in computing velocity signals of visual motion can give rise to perception of self-displacements.
By studying the effects of optic flow on the activity of MST neurons, evidence has been provided in monkey of a role in heading perception of this visual area Page and Duffy, ; Shenoy et al. Figure 2 shows an example of MST cells discharging to simple and distorted flow fields that simulate self-motion plus an eye movement Bremmer et al.
Bremmer et al. Responses of a single MST neuron to unidirectional motion and optic flow. A Polar plot of the directional selectivity to left and downward motion. B Receptive field RF characterized by moving luminant bars to the left. In the insets are shown the neuron responses in each condition. Note that the neurons is reliably responding to rightward heading leftward visual flow D,F and not to leftward heading rightward visual flow irrespective of the eye-movement-related distortion.
Reproduced from Bremmer et al. It is likely that MST yields a common cortical process sub-serving heading perception and optokinetic response generation, both elicited by large visual field displacements. Recent works Cardin and Smith, suggest that a subset of cortical regions, including MST, the ventral intraparietal area, the medial visual area V6 as well as the cingulate cortex could integrate stereoscopic visual cues into ego-motion information.
Neuroimaging using PET or fMRI approaches have demonstrated that human occipito-temporal cortex is engaged in the processing of retinal and extraretinal SP velocity as well as optokinetic signals Barton et al. In sum, MST neurons might contribute to distinguish between external versus self-induced motion. However, such a computation requires that the visual signals about the environment displacement and the vestibular signals about the body motion are integrated in this same cortical region.
The next section will show how combined with the visual signals, the vestibular signals about body motion will disambiguate ego-motion from object motion. As previously mentioned, extrastriate visual areas including MST, the medial area V6 and VIP, might participate in the encoding of combined retinal and extraretinal signals including vestibular signals related to head displacements.
Recently a series of electrophysiological experiments in monkey clearly demonstrate that these MSTd neurons were firing during optic flow as well as during vestibular stimulation, hence subtending heading perception in separate reference frames, respectively eye-centered and head-centered Fetsch et al. In the context of self-motion perception, the notion of an integration of vestibular signals in this extrastriate cortex then follows logically, and is clearly demonstrated via unit recordings in monkey after bilateral labyrinthectomy Takahashi et al.
Takahashi et al. Indeed, as illustrated in Figure 3 , many neurons in MSTd respond during vestibular stimulation in the dark and can display the same or opposite tuning for direction of motion in both visual and vestibular modalities, suggesting multimodal interactions in encoding heading Bremmer et al. Based on these findings, it is likely that the extrastriate visual area MST contributes to self-motion regulation in coupling visual and vestibular kinetic information in order to compensate for retinal slip and thereby to maintain world stability during ego-motion.
If evidence is provided of such MST influence on self-motion, it is not exclusive as visual and vestibular heading encoding has also been found in macaque ventral intraparietal area VIP; Bremmer et al. Vestibular and visual tuning of three MST neurons responding to heading directions defined respectively by inertial motion alone vestibular , optic flow alone visual , and congruent combinations of the two cues combined.
D Representations of the 3D heading directions in azimuth and elevation angles. A Neuron with congruent tuning for heading elicited by vestibular and visual cues.
B Neuron with incongruent tuning for heading elicited by vestibular and by visual cues. C Neuron with selective tuning for visual heading only. Reproduced from Gu et al. In humans, similar findings have been reported in a cortical network including the homolog of the motion sensitive areas MST i. However, using functional MRI, Cardin et al. While MST might provide a representation of heading perception, V6 would rather be concerned with obstacle avoidance during self-motion as inferred by Cardin et al.
By using galvanic stimulation in humans, Smith et al. Furthermore, by investigating the cortical activation elicited during vection, Brandt et al. Thus, in order to disambiguate self-motion from object motion, reciprocal excitatory-inhibitory influences would occur within cortical loops including visual extrastriate cortex MST and vestibularly activated cortex i. Brandt et al.
So far, if self-motion encoding seems to emerge from the activity of the superior temporal cortex, very few studies report on a possible top-down regulation by this region on visuo-vestibular-related structures. As described above, Dursteler and Wurtz have shown that chemical lesions in MST produce deficits in OKN induced by large visual field displacement. Otherwise, possible top-down influences are suggested by the existence of projections from the parieto-temporal cortex to the subcortical vestibular complex in monkey Ventre and Faugier-Grimaud, Interestingly, by analyzing the topography of the injection sites in the parieto-temporal cortex, MST might have been encroached upon by our injections including the postero-ventral part of the parietal cortex and the dorsal banks of the superior temporal sulcus Faugier-Grimaud and Ventre, As illustrated in Figure 4 these parieto-temporal cortical sites were found to be directly projecting onto the vestibular nuclei complex including the medial vestibular and PH nucleus involved in the velocity storage integrator and gaze holding processing Cheron et al.
Interestingly, the connections from some extrastriate visual areas including MST responsible for visual motion processing in the far periphery might mediate rapid-response related information for orienting and postural reactions Palmer and Rosa, Horseradish peroxidase HRP anterograde labeling in vestibular complex and prepositus hypoglossi in macaque monkey. A Schematic representation of the location of the HRP injection site in the parieto-temporal cortex. B,C Reconstruction of the labeled zones in the vestibular complex and in the prepositus hypoglossi.
In the bottom part, darkfield photomicrographs display bright labeled neurons and fibers in the medial M and superior S vestibular nuclei and in the prepositus hypoglosi nucleus PH.
Insets are showing the locations in the brainstem where the photomicrographs have been taken. Adapted from Ventre and Faugier-Grimaud As a whole, the extrastriate areas including the middle superior temporal area MST are clearly implicated in processing movement information during ego-motion. There, we will try to identify and assemble the functional features of this parieto-temporal region suggestive of integration e.
The first evidence of a pure vestibular cortical field was provided by evoked potentials techniques in the cat Walzl and Mountcastle, These authors showed that a neuronal activity could be evoked by vestibular nerve stimulation in an anterior area of the suprasylvian sulcus, anterior to the auditory area and to the motion analysis suprasylvian cortex previously described.
These observations in animal were in line with a temporal lobe hypothesis of a vestibular cortex suggested in human patients after cortical damage Carmichael et al.
By electrophysiological recordings in the cat and in the monkey Kornhuber and Da Fonseca, ; Fredrickson et al. A clear description of vestibular cortical fields were provided in behaving animals in the early s by Mergner in the cat anterior suprasylvian cortex and by Kawano and Sasaki , Kawano et al. Thus these electrophysiological recording studies provided evidence that vestibular inputs were integrated in cortex during sinusoidal rotation Becker et al.
In Java monkey, Grusser et al. The authors called this region the parieto-insular vestibular cortex PIVC which they demonstrated further to be directly connected to the vestibular nuclei complex in the brainstem Akbarian et al. Indeed, by using a unilateral cortical lesion approach Ventre and Faugier-Grimaud, , we demonstrated that unilateral damage of the postero-lateral part of area 7 in monkey induced vestibulo-ocular disturbances similar to those observed after a unilateral damage of the cortical homolog in the cat, the middle suprasylvian cortex Ventre, b.
Such top-down effects on vestibulo-oculomotor function were confirmed as we found direct projections from this parietal cortex previously lesioned: Ventre and Faugier-Grimaud, onto the vestibular nuclei complex as well as on the prepositus hypoglossi nucleus NPH in monkey Ventre and Faugier-Grimaud, , Faugier-Grimaud and Ventre, The existence of a large network of cortical areas projecting onto the vestibular nuclei was also demonstrated by further anatomical works in monkey Faugier-Grimaud and Ventre, ; Akbarian et al.
Figure 5 synthesizes the different findings related to cortical projections onto the vestibular nuclei complex and prepositus hypoglossi distinguishing ascending oculomotor projections from descending skeletto-motor projections. Therefore, in the posterior associative cortex of monkey, evidence was provided for two distinct sites: 1 a caudal site corresponding to the posterior part of area 7 and 2 a second more rostral site, in the retro insular cortex corresponding to the so-called PIVC.
In humans, a number of neuroimaging studies PET and fMRI investigated the cortical activation induced by caloric or galvanic stimulation of healthy subjects Bottini et al.
A neural network similar to the one described in monkey was found to be distributed between the parietal, temporal cortex and prefrontal cortices. While the postero-lateral part of the monkey parietal cortex is likely to correspond to the parieto-temporal cortex including area 39—40 on the parietal convexity Ventre and Faugier-Grimaud, , Faugier-Grimaud and Ventre, ; Kahane et al.
A number of neuro-imaging studies have suggested that the PIVC could correspond to the retro-insular cortex in humans Dieterich and Brandt, ; Fasold et al.
However, based on correlations between functional imaging and cytoarchitectonic data, such an analogy has been recently revisited Eickhoff et al. Accordingly, by using electrical stimulation in epilepsy patients, Kahane et al. Consequently, in the following we will refer to the parietal operculum i.
At this point of our knowledge related to the organization of the vestibular cortex in primate, a question can be raised: whether these two parietal cortex on the cortical surface vs. So far, even though numerous studies including human investigations confirm the parietal involvement in vestibular function, the exact functional contribution of its different fields TPJ vs OP2 remains unclear.
Schematic representation of the vestibular cortical sites directly connected to the vestibular nuclei and the prepositus hypoglossi in macaque brain. In the right panels: Projections topographically organized with the caudal vestibular cortical fields including MST, RI, and TPJ projecting more in the vestibular and prepositus hypoglossi nuclei, involved in the oculomotor ascending pathways green patches as compared to the more rostral cortical fields connected to the vestibular nuclei mainly involved in the skeletto-motor descending pathways red patches.
Prepositus hypoglossi PH nucleus. Reconstructed from previous findings from Ventre and Faugier-Grimaud , Akbarian et al. The temporo-parietal cortical junction constitutes a major hub of multi-sensory convergence and transformations underlying spatial representation.
Such a role of the parietal cortex in spatially oriented behavior has been revealed by the neglect syndrome that can develop in patients after right parietal damage for review, Karnath and Dieterich, ; Karnath and Rorden, A visuo-spatial neglect is a neurological disorder characterized by a difficulty for patients with a right brain injury to respond or orient themselves to persons or objects located in the contralesional space.
Neglect patients usually exhibit spontaneous and sustained deviation of their eyes and head toward the side of the brain damage. Interestingly this cortical perisylvian network partially overlaps with the temporo-peri-Sylvian vestibular network defined by Kahane et al. This peri-Sylvian vestibular network would preferentially process vestibular canal signals that transduce angular head accelerations Kahane et al.
The similarity in the topographical aspects of the neglect vs vestibular peri-sylvian networks is also paralleled with a similarity in behavioral deficits, i. Furthermore, it has been shown that a durable compensation of the neurological spatial disorders can occur after unilateral labyrinthine stimulation in neglect patients Rubens, ; Vallar et al.
In keeping with this idea of a linkage between parieto-temporal cortex, visuo-spatial, and vestibular functions, we have shown vestibulo-ocular deficits in patients with unilateral parieto-temporal lesions Ventre-Dominey et al. As illustrated in Figure 6 , the vestibular deficits were preeminent for the inertial components of the vestibulo-ocular reflex the time constant and bias and were significantly linked to visuo-spatial disorders Ventre-Dominey et al.
Accordingly, by using a novel paradigm combining bistable perceptual stimuli or complex attentional tasks with concurrent vestibular stimulation in healthy human subjects, Arshad et al. In a patient with a residual neglect consecutive to an occipito-parieto-temporal damage, the ability to update the contralesional visual space after angular rotation was perturbed Ventre-Dominey and Vallee, In normal subjects, Seemungal et al.
On the basis of these observations we infer that the parieto-temporal cortex exerts a down regulation of the vestibulo-ocular function in particular the inertial low frequency component implying the velocity storage integrator. Vestibulo-ocular VOR deficits observed in patients after unilateral lesions in the parieto-temporal junction.
R: right lesion without neglect. L: Left lesion. On the bottom, graphs showing the asymmetrical deficits in VOR time constant measured by the directional preponderance and the VOR bias in each patient group. The deficits are majored with right lesions with neglect. Adapted from Ventre-Dominey et al. Evidence for the top-down influence of the parieto-temporal cortex in primate is strengthened by the existence of direct anatomical pathways connecting this part of the posterior cortex to the vestibular nuclei complex Figure 4.
Indeed, we have demonstrated in monkey that the parietal cortex located posteriorly to the PIVC projects directly onto the vestibular nuclei including the medial vestibular and PH nuclei involved in the velocity storage integrator and gaze holding processing Cheron et al. Based on our findings and those of the recent literature, we suggest that the parietal cortex constitutes a unique cortical region involved in high-ordered multimodal transformation of inertial vestibular signals including the updating of the visual space during body displacements.
The idea of a vestibular influence in space representation involving the parieto-temporal cortex has been extended to self-referential processing by a series of experiments using illusory percepts Blanke and Arzy, ; Tsakiris and Haggard, ; Ionta et al. For example, the most commonly described experiment the so-called rubber-hand illusion demonstrates how a sensory conflict between visual and tactile signals can produce changes in bodily self-referential Tsakiris and Haggard, Interestingly, such an illusory perception of a false hand ownership is emphasized by galvanic vestibular stimulation using the same paradigm of the rubber-hand illusion Lopez et al.
Lopez et al. The vestibular cortex intimately interacts with the visual cortex to match the two 3-D orientation maps perception of verticality, room-tilt illusion and mediates self-motion perception by means of a reciprocal inhibitory visual-vestibular interaction.
This mechanism of an inhibitory interaction allows a shift of the dominant sensorial weight during self-motion perception from one sensory modality visual or vestibular to the other, depending on which mode of stimulation prevails: body acceleration vestibular input or constant velocity motion visual input. Abstract Evidence is presented that the multisensory parieto-insular cortex is the human homologue of the parieto-insular vestibular cortex PIVC in the monkey and is involved in the perception of verticality and self-motion.
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