Neurons in striate cortex limit the spatial and temporal resolution for detecting disparity modulation.

Stereopsis is the process of seeing depth constructed from binocular disparity. The human ability to perceive modulation of disparity over space (Tyler, 1974; Prince and Rogers, 1998; Banks et al., 2004a) and time (Norcia and Tyler, 1984) is surprisingly poor, compared with the ability to detect spatial and temporal modulation of luminance contrast. In order to examine the physiological basis of this poor spatial and temporal resolution of stereopsis, I quantified responses to disparity modulation in disparity selective V1 neurons from four awake behaving monkeys. To study the physiological basis of the spatial resolution of stereopsis, I characterized the three-dimensional structure of 55 V1 receptive fields (RF) using random dot stereograms in which disparity varied as a sinusoidal function of vertical position (“corrugations”). At low spatial frequencies, this produced a modulation in neuronal firing at the temporal frequency of the stimulus. As the spatial frequency increased, the modulation reduced. The mean response rate changed little, and was close to that produced by a uniform stimulus at the mean disparity of the corrugation. In 48/55 (91%) of the neurons, the modulation strength was a lowpass function of spatial frequency. These results suggest that the neurons have fronto-parallel planar receptive fields, no disparity-based surround inhibition and no selectivity for disparity gradients. This scheme predicts a relationship between RF size and the high frequency cutoff. Comparison with independent measurements of RF size was compatible with this. All of this behavior closely matches the binocular energy model, which functionally corresponds to cross-correlation: the disparity modulated activity of the binocular neuron measures the correlation between the filtered monocular images. To examine the physiological basis of the temporal resolution of stereopsis, I measured for 59 neurons the temporal frequency tuning with random dot stereograms in which disparity varied as a sinusoidal function of time. Temporal frequency tuning in response to disparity modulation was not correlated with temporal frequency tuning in response to contrast modulation, and had lower temporal frequency high cutoffs on average. The temporal frequency high cut for disparity modulation was negatively correlated with the response latency, the speed of the response onset and the temporal integration time (slope of the line relating response phase and temporal frequency). Binocular cross-correlation of the monocular images after bandpass filtering can explain all these results. Average peak temporal frequency in response to disparity modulation was 2Hz, similar to the values I found in four human observers (1.5-3Hz). The mean cutoff spatial frequency, 0.5 cpd, was similar to equivalent measures of decline in human psychophysical sensitivity for such depth corrugations as a function of frequency (Tyler, 1974; Prince and Rogers, 1998; Banks et al., 2004a). This suggests that the human temporal and spatial resolution for stereopsis is limited by selectivity of V1 neurons. For both, space and time, the lower resolution for disparity modulation than for contrast modulation can be explained by a single mechanism, binocular cross-correlation of the monocular images. The findings also represent a significant step towards understanding the process by which neurons solve the stereo correspondence problem (Julesz, 1971)

Visual System Development in People with One Eye: Behaviour and Structural Neural Correlates

Postnatal monocular deprivation from the surgical removal (enucleation) of one eye in humans results in intact spatial form vision, although its consequences on motion perception development are less clear. Changes in brain structure following early monocular enucleation have either been assessed in species whose visual system is quite different from humans, or in enucleated monkeys and humans following short-term survival. In this dissertation, I sought to determine the long-term effects of enucleation on visual system development by examining behavioural visual abilities and visual system morphology in adults who have had one eye enucleated early in life due to retinoblastoma. In Chapter II, I conducted a series of speed and luminance contrast discrimination tasks not yet implemented in this group. Early monocular enucleation results in impaired speed discrimination but intact contrast perception compared to binocular and monocular viewing controls. These findings suggest differential effects of enucleation on the development of spatial form vision and motion perception. In Chapters III and IV, I obtained high-resolution structural magnetic resonance images to assess the morphological development of subcortical (Chapter III) and cortical (Chapter IV) structures in the visual pathway. Early monocular enucleation resulted in decreased optic chiasm width and volume, optic tract diameters, and lateral geniculate nuclei (LGN) volumes compared with binocularly intact controls. Surprisingly, however, optic tract diameter and LGN volume decreases were less severe contralateral to the remaining eye. Early monocular enucleation also resulted in increased grey matter surface area of visual and non-visual cortices compared with binocularly intact controls. Consistent with the LGN asymmetry, increased surface area of the primary visual cortex was restricted to the hemisphere contralateral to the remaining eye. Surprisingly, however, these increases were found for those with right- but not left-eye enucleation, suggesting different developmental time periods for each hemisphere. Possible mechanisms of altered development following early monocular enucleation include: 1) recruitment of deafferented cells by the remaining eye, 2) retention of deafferented cells due to feedback from visual cortex, and 3) a disruption in synaptic pruning. These data highlight the importance of receiving normal levels of binocular visual input during infancy for typical visual development

fMRI studies of amblyopia: Pediatric and adult perspectives

Functional magnetic resonance imaging (fMRI) is currently the technique of choice for mapping functional neuroanatomy in humans, and over the past 15 years there has been a dramatic growth in the number of studies that provide brain-behavior correlations in normal healthy adults. More recently, a few studies have begun to make such measures in healthy children. In addition, fMRI is increasingly being applied to study brain function in subjects with neurological disease. The overall aim of these studies was to apply fMRI methods to the study of amblyopia, the most prevalent developmental vision disorder. Amblyopia develops early in life, usually before 5 years old, and is most treatable during childhood. Our approach was to study both children and adults with either the strabismic or the anisometropic type of amblyopia. In our first experiment (Chapter 3), we applied fMRI techniques to map retinotopic visual organization in children. We conclude that cortical visual organization is measurable and highly mature in children aged 9 to 12 years. In our second experiment (Chapter 4), we applied similar techniques to adults with amblyopia. We conclude that visual field organization is abnormal in the brains of these adults. In our final experiment (Chapter 5), we applied these same techniques to children with amblyopia, and observed abnormalities similar to those seen in adults. These studies present a novel neurological characterization of amblyopia, and provide a basis for further studies of human visual development, in health and disease

Parallel and serial processing of visual information in the brain: A review

Following the transduction of light by the photoreceptors in the retina, information about stimulus color and fine detail is separated from information about gross form and movement. Information regarding these stimulus characteristics is then carried via parallel pathways through the magno and parvo cellular layers of the geniculate to the cortex where it is analyzed in separate areas. This article reviews the parallel and serial analysis of visual information in the brain, and provides clinical examples illustrating failures in the analysis process

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

Perceptual plasticity in damaged adult visual systems

AbstractPlasticity appears to be a ubiquitous property of nervous systems, regardless of developmental stage or complexity. In the visual system of higher mammals, perceptual plasticity has been intensively studied, both during development and in adulthood. However, the last few years have seen some significant controversies arise about the existence and properties of visual plasticity after permanent damage to the adult visual system. The study of perceptual plasticity in damaged, adult visual systems is of interest for several reasons. First, it is an important means of unmasking the relative contribution of individual visual areas to visual learning, adaptation and priming, among other plastic phenomena. Second, it can provide knowledge that is essential for the development of effective therapies to rehabilitate the increasing number of people who suffer the functional consequences of damage at different levels of their visual hierarchy. This review summarizes the available evidence on the subject and proposes that visual plasticity may be just as ubiquitous after damage as it is in the intact visual system. However, damage may alter visual plasticity in ways that are still being defined

Étude électrophysiologique de la suppression interoculaire : implication pour l'amblyopie

L’amblyopie est un trouble développemental de la vision binoculaire. Elle est typiquement caractérisée par des atteintes de l’acuité visuelle et de la stéréoscopie. Toutefois, de plus en plus d’études indiquent la présence d’atteintes plus étendues telles que les difficultés d’attention visuelle ou de lecture. L’amblyopie est généralement expliquée par une suppression interoculaire au niveau cortical, considérée comme chronique ou permanente à l’extérieur de la période développementale. Or, un nombre croissant d’études suggèrent que des interactions binoculaires normales seraient présentes chez les amblyopes adultes. Dans une première étude, nous avons tenté d’identifier un marqueur électrophysiologique de la vision binoculaire. Nous avons enregistré des potentiels évoqués visuels chez des observateurs normaux à qui l’on a induit une dysfonction binoculaire. Les interactions binoculaires étaient caractérisées à l’aide de patrons (facilitation, moyennage et suppression) en comparant les réponses monoculaires et binoculaires. De plus, ces interactions étaient quantifiées à partir d’index d’intégration continus en soustrayant la somme des réponses monoculaires de la réponse binoculaire. Les résultats indiquaient que les patrons d’interaction n’étaient pas optimaux pour estimer les performances stéréoscopiques. Ces dernières étaient, en revanche, mieux expliquées par notre index d’intégration binoculaire. Ainsi, cette étude suggère que l’électrophysiologie est un bon prédicteur de la vision binoculaire. Dans une deuxième étude, nous avons examiné les corrélats neuronaux et comportementaux de la suppression interoculaire chez des amblyopes adultes et des observateurs normaux. Des potentiels évoqués visuels stationnaires ont été enregistrés en utilisant un paradigme de suppression par flash. La suppression était modulée par un changement de contraste du stimulus flash (10, 20, 30, ou 100%), ou le suppresseur, qui était présenté soit dans l’œil dominant ou non-dominant (ou amblyope). Sur le plan comportemental, la suppression interoculaire était observée indépendamment de l’œil stimulé par le flash chez les contrôles. Au contraire, chez les amblyopes, la suppression était asymétrique (c’est-à-dire supérieure lorsqu’elle provenait de l’œil dominant), ce qui suggérait une suppression chronique. De manière intéressante, l’œil amblyope a supprimé l’œil dominant à haut niveau de contraste. Sur le plan électrophysiologique, l’effet de suppression interoculaire observé à la région occipitale était équivalent dans chaque groupe. Toutefois, les réponses électrophysiologiques à la région frontale chez les amblyopes n’étaient pas modulées comme celles des contrôles; la suppression de l’œil amblyope était manifeste même à bas contraste. Nous résultats supportent ainsi l’existence d’interaction binoculaire fonctionnelle chez les amblyopes adultes ainsi que l’implication d’un réseau cortical étendu dans la suppression interoculaire. En somme, l’amblyopie est une condition complexe dont les atteintes corticales et les déficits fonctionnels semblent globaux. L’amblyopie ne doit plus être considérée comme limitée à une dysfonction de l’aire visuelle primaire. La suppression interoculaire semble un point central de cette problématique, mais encore beaucoup d’études seront nécessaires afin de déterminer l’ensemble des mécanismes impliqués dans celle-ci.Amblyopia is a developmental dysfunction of binocular vision. It is typically characterized by visual acuity and stereopsis deficits. However, presence of more spread deficits such as problems in visual attention and reading are beginning to be reported in literature. Amblyopia is generally explained by interocular suppression at cortical level, which is considered to be chronic or permanent outside the developmental period. Nevertheless, a growing body of evidence suggests that normal binocular interactions are still present in amblyopic adults. In the first study, we tried to establish an electrophysiological marker of binocular vision. Visual evoked potentials (VEPs) were recorded in normal observers for whom binocular dysfunction was induced. Patterns of binocular interaction were categorized (facilitation, averaging or suppression) by comparing monocular and binocular responses. Quantitative and continuous indexes of binocular integration were also calculated (binocular response minus the sum of monocular responses). Results indicated that patterns of interaction were not optimal to account for stereoscopic performance. The latter was, however, best explained by binocular integration indexes. This study shows evidence of predicting binocular vision based on a novel index that allows continuous quantification of binocular transient-VEP responses. In the second study, we examined the behavioural and neural correlates of interocular suppression in amblyopic adults and controls using a flash suppression paradigm while recording steady-state visual evoked potentials (ssVEP). The strength of suppression was manipulated by changing the contrast (10, 20, 30 or 100%) of the "flash", or the suppressor, and the stimulus was presented either in the dominant (or fellow) or non-dominant (or amblyopic) eye. At the behavioural level, interocular suppression was found regardless the eye origin of the flash for normal observers, but was asymmetric in the amblyopes, so that the suppression from the fellow eye was stronger, supporting a putative chronic suppression. Interestingly, the amblyopic eye suppressed the dominant eye at the highest contrast level. At the electrophysiology level, interocular suppression effects found over the occipital region were equivalent in both groups. However, ssVEP responses over the frontal region in the amblyopic observers were not modulated as those in controls; suppression of the amblyopic eye was manifest even at low contrast levels. Our findings support the existence of functional binocular interaction in adult amblyopia and the implication of a widespread cortical network in interocular suppression. To conclude, amblyopia is a complex condition with widespread cortical and functional deficits. It seems clear that it can’t be limited to a primary visual cortex dysfunction. Interocular suppression seems a core mechanism of the problematic, but more studies are necessary to determine more precise mechanisms implicated

Towards building a more complex view of the lateral geniculate nucleus: Recent advances in understanding its role

The lateral geniculate nucleus (LGN) has often been treated in the past as a linear filter that adds little to retinal processing of visual inputs. Here we review anatomical, neurophysiological, brain imaging, and modeling studies that have in recent years built up a much more complex view of LGN . These include effects related to nonlinear dendritic processing, cortical feedback, synchrony and oscillations across LGN populations, as well as involvement of LGN in higher level cognitive processing. Although recent studies have provided valuable insights into early visual processing including the role of LGN, a unified model of LGN responses to real-world objects has not yet been developed. In the light of recent data, we suggest that the role of LGN deserves more careful consideration in developing models of high-level visual processing

Binocular interactions in human vision

Early visual processing is subject to binocular interactions because cells in striate cortex show binocular responses and ocular dominance (Hubel & Weisel, 1968). The work presented in this thesis suggests that these physiological interactions can be revealed in psychophysical experiments using normal human observers. In the region corresponding to the blind spot, where binocular interactions differ from areas of the visual field which are represented by two eyes, monocular contrast sensitivity is increased. This finding can be partially explained by an absence of normal binocular interactions in this location (Chapter 2). A hemianopic patient was studied in an attempt to discover whether the effect in normal observers was mediated by either a mechanism in striate cortex or via a subcortical pathway. However, the results were unable to distinguish between these two explanations (Chapter 3).In a visual search task, no difference in reaction time was observed for targets presented to the region corresponding to the blind spot compared with targets presented to adjacent binocularly represented areas of the visual field. Since performance was unaffected by the monocularity of the region corresponding to the blind, pop-out for orientation may be mediated beyond striate cortex where cells are binocularly balanced (Chapter 5). Further support for this contention was provided by studies of orientation pop-out in central vision which found that dichoptic presentation of stimuli did not affect the degree of pop-out obtained and that in general, visual search for a target based solely on eye of origin is impossible (Chapter 6). However, a task that measured orientation difference sensitivity more directly than the search experiments, found that thresholds were higher for dichoptically presented stimuli. This suggests the involvement of neurons that receive a weighted input from each eye. A model of orientation difference coding can account for the results by assuming that the range of inhibition across which orientation differences are coded is narrower for dichoptic stimuli leading to a greater resolvable orientation difference (Chapter 7)

Towards a Unified Theory of Neocortex: Laminar Cortical Circuits for Vision and Cognition

A key goal of computational neuroscience is to link brain mechanisms to behavioral functions. The present article describes recent progress towards explaining how laminar neocortical circuits give rise to biological intelligence. These circuits embody two new and revolutionary computational paradigms: Complementary Computing and Laminar Computing. Circuit properties include a novel synthesis of feedforward and feedback processing, of digital and analog processing, and of pre-attentive and attentive processing. This synthesis clarifies the appeal of Bayesian approaches but has a far greater predictive range that naturally extends to self-organizing processes. Examples from vision and cognition are summarized. A LAMINART architecture unifies properties of visual development, learning, perceptual grouping, attention, and 3D vision. A key modeling theme is that the mechanisms which enable development and learning to occur in a stable way imply properties of adult behavior. It is noted how higher-order attentional constraints can influence multiple cortical regions, and how spatial and object attention work together to learn view-invariant object categories. In particular, a form-fitting spatial attentional shroud can allow an emerging view-invariant object category to remain active while multiple view categories are associated with it during sequences of saccadic eye movements. Finally, the chapter summarizes recent work on the LIST PARSE model of cognitive information processing by the laminar circuits of prefrontal cortex. LIST PARSE models the short-term storage of event sequences in working memory, their unitization through learning into sequence, or list, chunks, and their read-out in planned sequential performance that is under volitional control. LIST PARSE provides a laminar embodiment of Item and Order working memories, also called Competitive Queuing models, that have been supported by both psychophysical and neurobiological data. These examples show how variations of a common laminar cortical design can embody properties of visual and cognitive intelligence that seem, at least on the surface, to be mechanistically unrelated.National Science Foundation (SBE-0354378); Office of Naval Research (N00014-01-1-0624