Spatial and temporal integration of binocular disparity in the primate brain

Le système visuel du primate s'appuie sur les légères différences entre les deux projections rétiniennes pour percevoir la profondeur. Cependant, on ne sait pas exactement comment ces disparités binoculaires sont traitées et intégrées par le système nerveux. D'un côté, des enregistrements unitaires chez le macaque permettent d'avoir accès au codage neuronal de la disparité à un niveau local. De l'autre côté, la neuroimagerie fonctionnelle (IRMf) chez l'humain met en lumière les réseaux corticaux impliqués dans le traitement de la disparité à un niveau macroscopique mais chez une espèce différente. Dans le cadre de cette thèse, nous proposons d'utiliser la technique de l'IRMf chez le macaque pour permettre de faire le lien entre les enregistrements unitaires chez le macaque et les enregistrements IRMf chez l'humain. Cela, afin de pouvoir faire des comparaisons directes entre les deux espèces. Plus spécifiquement, nous nous sommes intéressés au traitement spatial et temporal des disparités binoculaires au niveau cortical mais aussi au niveau perceptif. En étudiant l'activité corticale en réponse au mouvement tridimensionnel (3D), nous avons pu montrer pour la première fois 1) qu'il existe un réseau dédié chez le macaque qui contient des aires allant au-delà du cluster MT et des aires environnantes et 2) qu'il y a des homologies avec le réseau trouvé chez l'humain en réponse à des stimuli similaires. Dans une deuxième étude, nous avons tenté d'établir un lien entre les biais perceptifs qui reflètent les régularités statistiques 3D ans l'environnement visuel et l'activité corticale. Nous nous sommes demandés si de tels biais existent et peuvent être reliés à des réponses spécifiques au niveau macroscopique. Nous avons trouvé de plus fortes activations pour le stimulus reflétant les statistiques naturelles chez un sujet, démontrant ainsi une possible influence des régularités spatiales sur l'activité corticale. Des analyses supplémentaires sont cependant nécessaires pour conclure de façon définitive. Néanmoins, nous avons pu confirmer de façon robuste l'existence d'un vaste réseau cortical répondant aux disparités corrélées chez le macaque. Pour finir, nous avons pu mesurer pour la première fois les points rétiniens correspondants au niveau du méridien vertical chez un sujet macaque qui réalisait une tâche comportementale (procédure à choix forcé). Nous avons pu comparer les résultats obtenus avec des données également collectées chez des participants humains avec le même protocole. Dans les différentes sections de discussion, nous montrons comment nos différents résultats ouvrent la voie à de nouvelles perspectives.The primate visual system strongly relies on the small differences between the two retinal projections to perceive depth. However, it is not fully understood how those binocular disparities are computed and integrated by the nervous system. On the one hand, single-unit recordings in macaque give access to neuronal encoding of disparity at a very local level. On the other hand, functional neuroimaging (fMRI) studies in human shed light on the cortical networks involved in disparity processing at a macroscopic level but with a different species. In this thesis, we propose to use an fMRI approach in macaque to bridge the gap between single-unit and fMRI recordings conducted in the non-human and human primate brain, respectively, by allowing direct comparisons between the two species. More specifically, we focused on the temporal and spatial processing of binocular disparities at the cortical but also at the perceptual level. Investigating cortical activity in response to motion-in-depth, we could show for the first time that 1) there is a dedicated network in macaque that comprises areas beyond the MT cluster and its surroundings and that 2) there are homologies with the human network involved in processing very similar stimuli. In a second study, we tried to establish a link between perceptual biases that reflect statistical regularities in the three-dimensional visual environment and cortical activity, by investigating whether such biases exist and can be related to specific responses at a macroscopic level. We found stronger activity for the stimulus reflecting natural statistics in one subject, demonstrating a potential influence of spatial regularities on the cortical activity. Further work is needed to firmly conclude about such a link. Nonetheless, we robustly confirmed the existence of a vast cortical network responding to correlated disparities in the macaque brain. Finally, we could measure for the first time retinal corresponding points on the vertical meridian of a macaque subject performing a behavioural task (forced-choice procedure) and compare it to the data we also collected in several human observers with the very same protocol. In the discussion sections, we showed how these findings open the door to varied perspectives

Synchronized Audio-Visual Transients Drive Efficient Visual Search for Motion-in-Depth

In natural audio-visual environments, a change in depth is usually correlated with a change in loudness. In the present study, we investigated whether correlating changes in disparity and loudness would provide a functional advantage in binding disparity and sound amplitude in a visual search paradigm. To test this hypothesis, we used a method similar to that used by van der Burg et al. to show that non-spatial transient (square-wave) modulations of loudness can drastically improve spatial visual search for a correlated luminance modulation. We used dynamic random-dot stereogram displays to produce pure disparity modulations. Target and distractors were small disparity-defined squares (either 6 or 10 in total). Each square moved back and forth in depth in front of the background plane at different phases. The target’s depth modulation was synchronized with an amplitude-modulated auditory tone. Visual and auditory modulations were always congruent (both sine-wave or square-wave). In a speeded search task, five observers were asked to identify the target as quickly as possible. Results show a significant improvement in visual search times in the square-wave condition compared to the sine condition, suggesting that transient auditory information can efficiently drive visual search in the disparity domain. In a second experiment, participants performed the same task in the absence of sound and showed a clear set-size effect in both modulation conditions. In a third experiment, we correlated the sound with a distractor instead of the target. This produced longer search times, indicating that the correlation is not easily ignored

Using Functional Near Infrared Spectroscopy (fNIRS) to study dynamic stereoscopic depth perception

The parietal cortex has been widely implicated in the processing of depth perception by many neuroimaging studies, yet functional near infrared spectroscopy (fNIRS) has been an under-utilised tool to examine the relationship of oxy- ([HbO]) and de-oxyhaemoglobin ([HbR]) in perception. Here we examine the haemodynamic response (HDR) to the processing of induced depth stimulation using dynamic random-dot-stereograms (RDS). We used fNIRS to measure the HDR associated with depth perception in healthy young adults (n = 13, mean age 24). Using a blocked design, absolute values of [HbO] and [HbR] were recorded across parieto-occipital and occipital cortices, in response to dynamic RDS. Control and test images were identical except for the horizontal shift in pixels in the RDS that resulted in binocular disparity and induced the percept of a 3D sine wave that 'popped out' of the test stimulus. The control stimulus had zero disparity and induced a 'flat' percept. All participants had stereoacuity within normal clinical limits and successfully perceived the depth in the dynamic RDS. Results showed a significant effect of this complex visual stimulation in the right parieto-occipital cortex (p < 0.01, η(2) = 0.54). The test stimulus elicited a significant increase in [HbO] during depth perception compared to the control image (p < 0.001, 99.99 % CI [0.008-0.294]). The similarity between the two stimuli may have resulted in the HDR of the occipital cortex showing no significant increase or decrease of cerebral oxygenation levels during depth stimulation. Cerebral oxygenation measures of [HbO] confirmed the strong association of the right parieto-occipital cortex with processing depth perception. Our study demonstrates the validity of fNIRS to investigate [HbO] and [HbR] during high-level visual processing of complex stimuli

Functional anatomy of stereoscopic visual process assessed using functional magnetic resonance imaging and structural equation modelling.

The purpose of this thesis is to study the functional anatomy of stereoscopic vision. Although many studies have investigated the physiological mechanisms by which the brain transforms the retinal disparities into three-dimensional representations, the invasive nature of the techniques available have restricted them to studies in non-human primates, whilst the research on humans has been limited to psychophysical studies. Modem non-invasive neuroimaging techniques now allow the investigation of the functional organisation of the human brain. Although PET and fMRI studies have been widely used, few researchers have explored the functional anatomy of stereoscopic vision. Most of these studies appear to be pilot work, showing inconsistency, not only in the areas sensitive to stereo disparities, but also in the specific role that each of these possesses in the perception of depth. In order to investigate the cortical regions involved in stereoscopic vision, four fMRI studies were performed using anaglyph random dot stereo grams. Our results suggest that the stereo disparity processing is widespread over a network of cortical regions which include VI, V3A, V3B and B7. Functionally, the V3A region seems to be the main processing centre of pure stereo disparities and the V3B region to be engaged in motion defined purely by spatio-temporal changes of local horizontal disparities (stereoscopic -cyclopean- motion). Interregional connectivity was investigated with two approaches. Structural Equation Modelling (SEM), as the classical technique for the analysis of effective connectivity, was used to assess one connectivity model proposed to· explain the cortical interaction observed in the first experiment. The implementation and application of this technique permitted us to identify some of its weaknesses in representing fMRI data. An extension of the SEM technique was introduced as a Non-linear Auto-Regressive Moving Average with eXogenous variables (NARMAX) approach. This can be thought of as an attempt to bring SEM towards a non-linear dynamic system modelling technique which permits a more appropriate representation of effective connectivity models using fMRI time series

Bistable Percepts in the Brain: fMRI Contrasts Monocular Pattern Rivalry and Binocular Rivalry

The neural correlates of binocular rivalry have been actively debated in recent years, and are of considerable interest as they may shed light on mechanisms of conscious awareness. In a related phenomenon, monocular rivalry, a composite image is shown to both eyes. The subject experiences perceptual alternations in which the two stimulus components alternate in clarity or salience. The experience is similar to perceptual alternations in binocular rivalry, although the reduction in visibility of the suppressed component is greater for binocular rivalry, especially at higher stimulus contrasts. We used fMRI at 3T to image activity in visual cortex while subjects perceived either monocular or binocular rivalry, or a matched non-rivalrous control condition. The stimulus patterns were left/right oblique gratings with the luminance contrast set at 9%, 18% or 36%. Compared to a blank screen, both binocular and monocular rivalry showed a U-shaped function of activation as a function of stimulus contrast, i.e. higher activity for most areas at 9% and 36%. The sites of cortical activation for monocular rivalry included occipital pole (V1, V2, V3), ventral temporal, and superior parietal cortex. The additional areas for binocular rivalry included lateral occipital regions, as well as inferior parietal cortex close to the temporoparietal junction (TPJ). In particular, higher-tier areas MT+ and V3A were more active for binocular than monocular rivalry for all contrasts. In comparison, activation in V2 and V3 was reduced for binocular compared to monocular rivalry at the higher contrasts that evoked stronger binocular perceptual suppression, indicating that the effects of suppression are not limited to interocular suppression in V1

Straight or curved? From deterministic to probabilistic models of 3D motion perception

A commentary on Detection of 3D curved trajectories: the role of binocular disparity by Pierce, R. S., Bian, Z., Braunstein, M. L., and Andersen, G. J. (2013). Front. Behav. Neurosci. 7:12. doi: 10.3389/fnbeh.2013.0001

fMRI correlates of subjective reversals in ambiguous structure-from-motion

We used fMRI to examine the neural correlates of subjective reversals for bistable structure-from-motion. We compared transparent random-dot kinematograms depicting either a cylinder rotating in depth or two flat surfaces translating in opposite directions at apparently different depths. For both such stimuli, the motion of dots on the different apparent depth planes typically appears to reverse direction periodically on prolonged viewing. Yet for cylindrical but not flat stimuli, such subjective reversals also coincide with apparent reversal of 3D rotation direction. We hypothesized that the lateral occipital complex (region LOC), sensitive to 3D form, might show greater event-related activity for subjective reversals of cylindrical than flat stimuli; conversely, motion-sensitive hMT+/V5 should respond in common to subjective reversals for either type of stimuli, as both are perceived as changes in planar motion. We obtained an event-related measure of neural activity associated with subjective reversals after first factoring out block-related differences between cylindrical versus flat stimuli (and thereby the associated low-level blocked stimulus differences). In support of our hypothesis, only the cylindrical stimuli produced reversal-related activity in contralateral human LOC. In contrast, the hMT+/V5 complex was activated alike by subjective reversals for both cylindrical and flat stimuli. Intriguingly, V1 also showed (contralateral) specificity for rotational reversals, suggesting a possible feedback influence from LOC. These results reveal specific neural correlates for subjective switches of 3D rotation versus translation, as distinct from subjective reversals in general

Organisation of audio-visual three-dimensional space

Le terme stéréopsie renvoie à la sensation de profondeur qui est perçue lorsqu une scène est vue de manière binoculaire. Le système visuel s appuie sur les disparités horizontales entre les images projetées sur les yeux gauche et droit pour calculer une carte des différentes profondeurs présentes dans la scène visuelle. Il est communément admis que le système stéréoscopique est encapsulé et fortement contraint par les connexions neuronales qui s étendent des aires visuelles primaires (V1/V2) aux aires intégratives des voies dorsales et ventrales (V3, cortex temporal inférieur, MT). A travers quatre projets expérimentaux, nous avons étudié comment le système visuel utilise la disparité binoculaire pour calculer la profondeur des objets. Nous avons montré que le traitement de la disparité binoculaire peut être fortement influencé par d autres sources d information telles que l occlusion binoculaire ou le son. Plus précisément, nos résultats expérimentaux suggèrent que : (1) La stéréo de da Vinci est résolue par un mécanisme qui intègre des processus de stéréo classiques (double fusion), des contraintes géométriques (les objets monoculaires sont nécessairement cachés à un œil, par conséquent ils sont situés derrière le plan de l objet caché) et des connaissances à priori (une préférence pour les faibles disparités). (2) Le traitement du mouvement en profondeur peut être influencé par une information auditive : un son temporellement corrélé avec une cible définie par le mouvement stéréo peut améliorer significativement la recherche visuelle. Les détecteurs de mouvement stéréo sont optimalement adaptés pour détecter le mouvement 3D mais peu adaptés pour traiter le mouvement 2D. (3) Grouper la disparité binoculaire avec un signal auditif dans une dimension orthogonale (hauteur tonale) peut améliorer l acuité stéréo d approximativement 30%Stereopsis refers the perception of depth that arises when a scene is viewed binocularly. The visual system relies on the horizontal disparities between the images from the left and right eyes to compute a map of the different depth values present in the scene. It is usually thought that the stereoscopic system is encapsulated and highly constrained by the wiring of neurons from the primary visual areas (V1/V2) to higher integrative areas in the ventral and dorsal streams (V3, inferior temporal cortex, MT). Throughout four distinct experimental projects, we investigated how the visual system makes use of binocular disparity to compute the depth of objects. In summary, we show that the processing of binocular disparity can be substantially influenced by other types of information such as binocular occlusion or sound. In more details, our experimental results suggest that: (1) da Vinci stereopsis is solved by a mechanism that integrates classic stereoscopic processes (double fusion), geometrical constraints (monocular objects are necessarily hidden to one eye, therefore they are located behind the plane of the occluder) and prior information (a preference for small disparities). (2) The processing of motion-in-depth can be influenced by auditory information: a sound that is temporally correlated with a stereomotion defined target can substantially improve visual search. Stereomotion detectors are optimally suited to track 3D motion but poorly suited to process 2D motion. (3) Grouping binocular disparity with an orthogonal auditory signal (pitch) can increase stereoacuity by approximately 30%PARIS5-Bibliotheque electronique (751069902) / SudocSudocFranceF

A Bayesian approach to the aperture problem of 3D motion perception

We suggest a geometric-statistical approach that can be ap- plied to the 3D aperture problem of motion perception. In simulations and psychophysical experiments we study per- ceived 3D motion direction in a binocular viewing geometry by systematically varying 3D orientation of a line stimulus moving behind a circular aperture. Although motion direc- tion is inherently ambiguous perceived directions show sys- tematic trends and a Bayesian model with a prior for small depth followed by slow motion in 3D gives reasonable fits to individual data. We conclude that the visual system tries to minimize velocity in 3D but that earlier disparity processing strongly influences perceived 3D motion direction. We discuss implications for the integration of disparity and motion cues in the human visual system

Vergence eye movements in patients with schizophrenia

AbstractPrevious studies have shown that smooth pursuit eye movements are impaired in patients with schizophrenia. However, under normal viewing conditions, targets move not only in the frontoparallel plane but also in depth, and tracking them requires both smooth pursuit and vergence eye movements. Although previous studies in humans and non-human primates suggest that these two eye movement subsystems are relatively independent of one another, to our knowledge, there have been no prior studies of vergence tracking behavior in patients with schizophrenia. Therefore, we have investigated these eye movements in patients with schizophrenia and in healthy controls. We found that patients with schizophrenia exhibited substantially lower gains compared to healthy controls during vergence tracking at all tested speeds (e.g. 0.25Hz vergence tracking mean gain of 0.59 vs. 0.86). Further, consistent with previous reports, patients with schizophrenia exhibited significantly lower gains than healthy controls during smooth pursuit at higher target speeds (e.g. 0.5Hz smooth pursuit mean gain of 0.64 vs. 0.73). In addition, there was a modest (r≈0.5), but significant, correlation between smooth pursuit and vergence tracking performance in patients with schizophrenia. Our observations clearly demonstrate substantial vergence tracking deficits in patients with schizophrenia. In these patients, deficits for smooth pursuit and vergence tracking are partially correlated suggesting overlap in the central control of smooth pursuit and vergence eye movements