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

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    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

    The medial parietal occipital areas in the macaque monkey

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    The number, location, extent, and functional properties of the cortical areas that occupy the medial parieto-occipital cortex (mPOC) have been, and still is, a matter of scientific debate. The mPOC is a convoluted region of the brain that presents a high level of individual variability, and the fact that many areas of mPOC are located within very deep sulci further limits the possibility to investigate their anatomo-functional properties. In the present review, we summarize the location and extent of mPOC areas in the macaque brain as obtained by architectural, connectional, and functional data. The different approaches lead to a subdivision of mPOC that includes areas V2, V3, V6, V6Av, and V6Ad. Extrastriate areas V2 and V3 occupy the posterior wall of the parieto-occipital sulcus (POs). The fundus of POs and the ventralmost part of the anterior wall of the sulcus are occupied by a retinotopically organized visual area, called V6, which represents the contralateral part of the visual field and emphasizes its periphery. The remaining part of the anterior wall of POs is occupied by two areas, V6Av and V6Ad, which contain visual as well as arm reaching neurons. Our analyses suggest that areas V6 and V6Av, together, occupy the cortical territory previously described as area PO. Functionally, area V6 is a motion area particularly sensitive to the real motion of objects in the animal's field of view, while V6Av and V6Ad are visuomotor areas likely involved in the visual guidance of arm movement and object prehension

    Visuospatial attention, motor intention, action affordance and brain plasticity: neurophysiology and network analysis

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    The project addresses sensorimotor integration for motor intention and execution within a unitary perspective, based on the assumption that the underlying processes can only be understood if considered as different aspects of a unitary mental construct, enabling non-human primates and humans to deploy attention and encode command functions to move and act effortlessly in the extra-personal space. The core objectives of the project concern: a) cortical encoding of kinetics and kinematics of grasping and reaching, their coupling during coordinated action, and action recognition when performed by another agent; b) the analysis of the memory reservoirs which help planning future action based on previous experience; c) how complex motor cortical circuits generate ethologically relevant forms of behavior; d) brain encoding of action affordances; e) the mechanisms necessary to allocate attention to a salient target, while resisting distractors, as a necessary prerequisite for successful action planning and performance. The statistical analysis of the distributed cortical system responsible for these functions will unravel the anatomical substrates of the above mentioned functions. Our approach will combine behavioral neurophysiology and neuroanatomy in monkeys, and will also include neurophysiological studies in humans. Neural activity (single unit, multi-unit, local field potentials) in different frontal, parietal and extrastriate cortical areas, including some of their subcortical targets such as the putamen, will be studied while monkeys perform ad hoc tasks assumed to recruit these areas, and inspired by their anatomical input and by the consequences of their lesion on behavior. These studies will not only be of correlative nature, but will also include the complex analysis of the causal relations between neural activity and behavior, through reversible inactivation of specific cortical sites in behaving animals. Cutting-edge experimental techniques will also be adopted in humans as well, where motor cortex will be electrically stimulated during neurosurgery in awake patients at behaviorally-relevant time scales, to study how ethologically relevant actions are generated, how their repeated performance affects cortical circuits, and how the wiring diagram of the cortical motor output can be reshaped by (hand) use. The relevance of these studies of sensorimotor control for the rehabilitation of skilled hand action as consequence of brain lesion is direct. Beyond the obvious statement that understanding brain function is essential to understand brain dysfunction, our project aims at conveying the message that this can only be feasible at multi-scale level, i.e. the micro-scale of cell function, the meso-scale level of cortical circuits, and the macro-scale level of behavioral analysis

    The human cortical areas V6 and V6A

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    In macaque, it has long been known since the late nineties that the medial parieto-occipital sulcus (POS) contains two regions, V6 and V6A, important for visual motion and action. While V6 is a retinotopically organized extrastriate area, V6A is a broadly retinotopically organized visuomotor area constituted by a ventral and dorsal subdivision (V6Av and V6Ad), both containing arm movement-related cells active during spatially directed reaching movements. In humans, these areas have been mapped only in recent years thanks to neuroimaging methods. In a series of brain mapping studies, by using a combination of functional magnetic resonance imaging methods such as wide-field retinotopy and task-evoked activity, we mapped human areas V6 (Pitzalis et al., 2006) and V6Av (Pitzalis et al., 2013 d) retinotopically and defined human V6Ad functionally as a pointing-selective region situated anteriorly in the close proximity of V6Av (Tosoni et al., 2014). Like in macaque, human V6 is a motion area (e.g., Pitzalis et al., 2010, 2012, 2013 a, b , c ), while V6Av and V6Ad respond to pointing movements (Tosoni et al., 2014). The retinotopic organization (when present), anatomical position, neighbor relations, and functional properties of these three areas closely resemble those reported for macaque V6 (Galletti et al., 1996, 1999 a), V6Av, and V6Ad (Galletti et al., 1999 b; Gamberini et al., 2011). We suggest that information on objects in depth which are translating in space, because of the self-motion, is processed in V6 and conveyed to V6A for evaluating object distance in a dynamic condition such as that created by self-motion, so to orchestrate the eye and arm movements necessary to reach or avoid static and moving objects in the environment

    Superior Parietal Lobule (SPL)

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    The posterior parietal cortex, in turn, is divided into superior (SPL) and inferior (IPL) parietal lobules, separated by the intraparietal sulcus. According to Brodmann (1909), the superior parietal lobule, the target of the present chapter, hosts two cytoarchitectonic fields, area 5 anteriorly and area 7 posteriorly. In the human brain, area 5 is a quite restricted area while area 7 occupies most of the SPL (see close-up in Fig. 1a). In the macaque brain, instead, area 5 occupies most of the SPL and area 7 only a restricted region of cortex in the caudalmost part of SPL (see close-up in Fig. 1b). Several studies in the last century claimed that this latter cortical region is not area 7, as originally indicated by Brodmann, but a variation of area 5. In either cases, it remains that the cytoarchitecture in SPL is not uniform, and the different architectural patterns of anterior and posterior parts of SPL suggest that they host different functional properties and subserve different functional roles.The following is a summary of the functional properties, anatomical connections, and possiblefunctional roles of SPL. The description refers to the macaque SPL, which has been intensively studied in the last decades. The human SPL has been much less studied to date and has not been taken into account here

    Neural activity in the medial parietal area V6A while grasping with or without visual feedback

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    Recent works have reported that grasping movements are controlled not only by the dorsolateral visual stream, as generally thought, but also by the dorsomedial visual stream, and in particular by the medial posterior parietal area V6A. To date, the grasping activity of V6A neurons has been studied only in darkness. Here we studied the effect of visual feedback on grasp-related discharges of V6A neurons while the monkey was preparing and executing the grasping of a handle. We found that V6A grasping activity could be excited or inhibited by visual information. The neural population was divided into Visual, Motor, and Visuomotor cells. The majority of Visual and Visuomotor neurons did not respond to passive observation of the handle, suggesting that vision of action, rather than object vision, is the most effective factor. The present findings highlight the role of the dorsomedial visual stream in integrating visual and motor signals to monitor and correct grasping

    Temporal stability of reference frames in monkey area V6A during a reaching task in 3D space

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    Neurons in the posterior parietal cortex of macaques show spatial tuning during several phases of an instructed delay reaching task, but their reference frames have been studied mostly during fixed periods without addressing how they evolve across task phases. In parietal area V6A, we reported recently that during the late delay and hand movement periods, most neurons represent target location either in body-centered frame of reference, or in mixed body/hand-centered coordinates, with no evidence of hand-centered representations. Here, we characterized the spatial representations of V6A neurons in earlier task epochs, i.e., immediately after target fixation and in the subsequent main part of the delay and examined whether the reference frames of individual neurons are stable across the task. We report no evidence of hand-centered coding also in the earlier phases of the task. Shortly, after target fixation and throughout the main part of the delay period, V6A neurons used either body-centered or mixed body/hand-centered reference frames. Most of the cells showed consistent reference frames across epochs. Interestingly, a population trend of shifting from mixed body/hand-centered frames to ‘pure’ body-centered coordinates was found as the task progressed. These findings suggest that, similar to other parietal areas, in V6A, the reference frames show a limited degree of temporal evolution. The stronger presence of mixed coding at the early task stages could reflect the early involvement of V6A in eye-hand coordination, whereas the increase in spatiotopic representations towards movement execution could be related to its role in online movement control

    Vision for Prehension in the Medial Parietal Cortex

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    In the last 2 decades, the medial posterior parietal area V6A has been extensively studied in awake macaque monkeys for visual and somatosensory properties and for its involvement in encoding of spatial parameters for reaching, including arm movement direction and amplitude. This area also contains populations of neurons sensitive to grasping movements, such as wrist orientation and grip formation. Recent work has shown that V6A neurons also encode the shape of graspable objects and their affordance. In other words, V6A seems to encode object visual properties specifically for the purpose of action, in a dynamic sequence of visuomotor transformations that evolve in the course of reach-to-grasp action.We propose a model of cortical circuitry controlling reach-to-grasp actions, in which V6A acts as a comparator that monitors differences between current and desired hand positions and configurations. This error signal could be used to continuously update the motor output, and to correct reach direction, hand orientation, and/or grip aperture as required during the act of prehension.In contrast to the generally accepted view that the dorsomedial component of the dorsal visual stream encodes reaching, but not grasping, the functional properties of V6A neurons strongly suggest the view that this area is involved in encoding all phases of prehension, including grasping
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