The Human Homologue of Macaque Area V6A

In macaque monkeys, V6A is a visuomotor area located in the anterior bank of the POs, dorsal and anterior to retinotopically-organized extrastriate area V6 (Galletti et al 1996). Unlike V6, V6A represents both contra- and ipsilateral visual fields and is broadly retinotopically organized (Galletti et al 1999b). The contralateral lower visual field is over-represented in V6A. The central 20°-30° of the visual field are mainly represented dorsally (V6Ad) and the periphery ventrally (V6Av), at the border with V6. Both sectors of area V6A contain arm movement-related cells, active during spatially-directed reaching movements (Gamberini et al., 2011). In humans, we previously mapped the retinotopic organization of area V6 (Pitzalis et al., 2006). Here, using phase-encoded fMRI, cortical surface-based analysis and wide-field retinotopic mapping, we define a new cortical region that borders V6 anteriorly and shows a clear over-representation of the contralateral lower visual field and of the periphery. As with macaque V6A, the eccentricity increases moving ventrally within the area. The new region contains a non-mirror-image representation of the visual field. Functional mapping reveals that, as in macaque V6A, the new region, but not the nearby area V6, responds during finger pointing and reaching movements. Based on similarity in position, retinotopic properties, functional organization and relationship with the neighbouring extrastriate visual areas, we propose that the new cortical region is the human homologue of macaque area V6A

Resting-state connectivity and functional specialization in human medial parieto-occipital cortex

According to recent models of visuo-spatial processing, the medial parieto-occipital cortex is a crucial node of the dorsal visual stream. Evidence from neurophysiological studies in monkeys has indicated that the parieto-occipital sulcus (POS) contains three functionally and cytoarchitectonically distinct areas: the visual area V6 in the fundus of the POS, and the visuo-motor areas V6Av and V6Ad in a progressively dorsal and anterior location with respect to V6. Besides different topographical organization, cytoarchitectonics, and functional properties, these three monkey areas can also be distinguished based on their patterns of cortico-cortical connections. Thanks to wide-field retinotopic mapping, areas V6 and V6Av have been also mapped in the human brain. Here, using a combined approach of resting-state functional connectivity and task-evoked activity by fMRI, we identified a new region in the anterior POS showing a pattern of functional properties and cortical connections that suggests a homology with the monkey area V6Ad. In addition, we observed distinct patterns of cortical connections associated with the human V6 and V6Av which are remarkably consistent with those showed by the anatomical tracing studies in the corresponding monkey areas. Consistent with recent models on visuo-spatial processing, our findings demonstrate a gradient of functional specialization and cortical connections within the human POS, with more posterior regions primarily dedicated to the analysis of visual attributes useful for spatial navigation and more anterior regions primarily dedicated to analyses of spatial information relevant for goal-directed action

Three-dimensional eye position signals shape both peripersonal space and arm movement activity in the medial posterior parietal cortex

Research conducted over the last decades has established that the medial part of posterior parietal cortex (PPC) is crucial for controlling visually guided actions in human and non-human primates. Within this cortical sector there is area V6A, a crucial node of the parietofrontal network involved in arm movement control in both monkeys and humans. However, the encoding of action-in-depth by V6A cells had been not studied till recently. Recent neurophysiological studies show the existence in V6A neurons of signals related to the distance of targets from the eyes. These signals are integrated, often at the level of single cells, with information about the direction of gaze, thus encoding spatial location in 3D space. Moreover, 3D eye position signals seem to be further exploited at two additional levels of neural processing: (a) in determining whether targets are located in the peripersonal space or not, and (b) in shaping the spatial tuning of arm movement related activity toward reachable targets. These findings are in line with studies in putative homolog regions in humans and together point to a role of medial PPC in encoding both the vergence angle of the eyes and peripersonal space. Besides its role in spatial encoding also in depth, several findings demonstrate the involvement of this cortical sector in non-spatial processes

Functional organization of the caudal part of the human superior parietal lobule

: Like in macaque, the caudal portion of the human superior parietal lobule (SPL) plays a key role in a series of perceptive, visuomotor and somatosensory processes. Here, we review the functional properties of three separate portions of the caudal SPL, i.e., the posterior parieto-occipital sulcus (POs), the anterior POs, and the anterior part of the caudal SPL. We propose that the posterior POs is mainly dedicated to the analysis of visual motion cues useful for object motion detection during self-motion and for spatial navigation, while the more anterior parts are implicated in visuomotor control of limb actions. The anterior POs is mainly involved in using the spotlight of attention to guide reach-to-grasp hand movements, especially in dynamic environments. The anterior part of the caudal SPL plays a central role in visually guided locomotion, being implicated in controlling leg-related movements as well as the four limbs interaction with the environment, and in encoding egomotion-compatible optic flow. Together, these functions reveal how the caudal SPL is strongly implicated in skilled visually-guided behaviors

Structural connectivity and functional properties of the macaque superior parietal lobule

Despite the consolidated belief that the macaque superior parietal lobule (SPL) is entirely occupied by Brodmann’s area 5, recent data show that macaque SPL also hosts a large cortical region with structural and functional features similar to that of Brodmann’s area 7. According to these data, the anterior part of SPL is occupied by a somatosensory-dominated cortical region that hosts three architectural and functional distinct regions (PE, PEci, PEip) and the caudal half of SPL by a bimodal somato-visual region that hosts four areas: PEc, MIP, PGm, V6A. To date, the most studied areas of SPL are PE, PEc, and V6A. PE is essentially a high-order somatomotor area, while PEc and V6A are bimodal somatomotor–visuomotor areas, the former with predominant somatosensory input and the latter with predominant visual input. The functional properties of these areas and their anatomical connectivity strongly suggest their involvement in the control of limb movements. PE is suggested to be involved in the preparation/execution of limb movements, in particular, the movements of the upper limb; PEc in the control of movements of both upper and lower limbs, as well as in their interaction with the visual environment; V6A in the control of reach-to-grasp movements performed with the upper limb. In humans, SPL is traditionally considered to have a different organization with respect to macaques. Here, we review several lines of evidence suggesting that this is not the case, showing a similar structure for human and non-human primate SPLs

Optic Ataxia: From Balint’s Syndrome to the Parietal Reach Region

Optic ataxia is a high-order deficit in reaching to visual goals that occurs with posterior parietal cortex (PPC) lesions. It is a component of Balint’s syndrome that also includes attentional and gaze disorders. Aspects of optic ataxia are misreaching in the contralesional visual field, difficulty preshaping the hand for grasping, and an inability to correct reaches online. Recent research in nonhuman primates (NHPs) suggests that many aspects of Balint’s syndrome and optic ataxia are a result of damage to specific functional modules for reaching, saccades, grasp, attention, and state estimation. The deficits from large lesions in humans are probably composite effects from damage to combinations of these functional modules. Interactions between these modules, either within posterior parietal cortex or downstream within frontal cortex, may account for more complex behaviors such as hand-eye coordination and reach-to-grasp

The dorsal visual stream revisited: Stable circuits or dynamic pathways?

In both macaque and human brain, information regarding visual motion flows from the extrastriate area V6 along two different paths: a dorsolateral one towards areas MT/V5, MST, V3A, and a dorsomedial one towards the visuomotor areas of the superior parietal lobule (V6A, MIP, VIP). The dorsolateral visual stream is involved in many aspects of visual motion analysis, including the recognition of object motion and self motion. The dorsomedial stream uses visual motion information to continuously monitor the spatial location of objects while we are looking and/or moving around, to allow skilled reaching for and grasping of the objects in structured, dynamically changing environments. Grasping activity is present in two areas of the dorsal stream, AIP and V6A. Area AIP is more involved than V6A in object recognition, V6A in encoding vision for action. We suggest that V6A is involved in the fast control of prehension and plays a critical role in biomechanically selecting appropriate postures during reach to grasp behaviors.In everyday life, numerous functional networks, often involving the same cortical areas, are continuously in action in the dorsal visual stream, with each network dynamically activated or inhibited according to the context. The dorsolateral and dorsomedial streams represent only two examples of these networks. Many others streams have been described in the literature, but it is worthwhile noting that the same cortical area, and even the same neurons within an area, are not specific for just one functional property, being part of networks that encode multiple functional aspects. Our proposal is to conceive the cortical streams not as fixed series of interconnected cortical areas in which each area belongs univocally to one stream and is strictly involved in only one function, but as interconnected neuronal networks, often involving the same neurons, that are involved in a number of functional processes and whose activation changes dynamically according to the context

Fix Your Eyes in the Space You Could Reach: Neurons in the Macaque Medial Parietal Cortex Prefer Gaze Positions in Peripersonal Space

Interacting in the peripersonal space requires coordinated arm and eye movements to visual targets in depth. In primates, the medial posterior parietal cortex (PPC) represents a crucial node in the process of visual-to-motor signal transformations. The medial PPC area V6A is a key region engaged in the control of these processes because it jointly processes visual information, eye position and arm movement related signals. However, to date, there is no evidence in the medial PPC of spatial encoding in three dimensions. Here, using single neuron recordings in behaving macaques, we studied the neural signals related to binocular eye position in a task that required the monkeys to perform saccades and fixate targets at different locations in peripersonal and extrapersonal space. A significant proportion of neurons were modulated by both gaze direction and depth, i.e., by the location of the foveated target in 3D space. The population activity of these neurons displayed a strong preference for peripersonal space in a time interval around the saccade that preceded fixation and during fixation as well. This preference for targets within reaching distance during both target capturing and fixation suggests that binocular eye position signals are implemented functionally in V6A to support its role in reaching and grasping

The posterior parietal area V6A: an attentionally-modulated visuomotor region involved in the control of reach-to-grasp action

In the macaque, the posterior parietal area V6A is involved in the control of all phases of reach-to-grasp actions: the transport phase, given that reaching neurons are sensitive to the direction and amplitude of arm movement, and the grasping phase, since reaching neurons are also sensitive to wrist orientation and hand shaping. Reaching and grasping activity are corollary discharges which, together with the somatosensory and visual signals related to the same movement, allow V6A to act as a state estimator that signals discrepancies during the motor act in order to maintain consistency between the ongoing movement and the desired one. Area V6A is also able to encode the target of an action because of gaze-dependent visual neurons and real-position cells. Here, we advance the hypothesis that V6A also uses the spotlight of attention to guide goal-directed movements of the hand, and hosts a priority map that is specific for the guidance of reaching arm movement, combining bottom-up inputs such as visual responses with top-down signals such as reaching plans

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