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Visuomotor integration in the medial parietal cortical areas
Visuomotor integration in the medial parietal cortical area
MIP for Action
The MIPforAction project, supported by the EU Marie Skłodowska Curie International Outgoing Action, addressed fundamental questions regarding the organization of primate parietal association cortex. The surface area of parietal cortex has expanded greatly in primates (including humans), and parietal subregions have no clear homologues in other mammals. We employed a multidisciplinary approach, making use of established anatomical and physiological methodologies, to study anatomical and functional characteristics of parietal cortex in monkeys. In addition, we used digital reconstructions of the brain surface as a means of visualization of cortical morphology and experimental data.
The medial parietal cortex plays a key role in our ability to interact with the environment using our limbs, as demonstrated by the consequences of damage to this part of the brain. Although it is recognized that medial parietal cortex likely contains different architectonic areas, it still remains one of the least characterized brain regions. Ongoing work in non-human primates has revealed medial parietal regions (see attached Figure) specialized for particular sensorimotor actions, such as reaching and grasping; however, the exact contributions of different areas to sensorimotor behavior remain unclear. Moreover, the recent advances in non-invasive research in humans, which suggest the existence of parallel networks for limb actions in the human brain, emphasize the need for detailed descriptions of the cortical areas involved in coordinating skilled arm movements.
The project aimed to provide a refined model of these areas, using anatomical tracing, histological reconstructions, and electrophysiological mapping of sensory activity. The main findings are as follows: First, medial parietal cortical areas form widespread connections with several brain areas, in the frontal, temporal, limbic, and local parietal cortices, emphasizing the associative features of the medial parietal cortex region. Second, the associative (i.e., neither strictly sensory nor motor) nature of this cortical sector is further suggested by the absence of connections with primary sensory cortices and general lack of purely sensory responses. Third, although links to premotor frontal cortex have been important in establishing the parietofrontal networks for limb movements, connections with less-studied parts of the brain are more difficult to interpret; for example, posterior temporal-parietal networks could possibly be related to shifts of attention to salient parts of the world, upon which an action might be directed. Fourth, by and large, the posterior parietal region appears to contain histologically defined areas with some overlap in connectivity patterns and function, adding to current theories of distributed information processing. In summary, present data, combined with our previous work on adjacent superior parietal areas, have provided a systematic view of the organization of cortical areas-components of networks for purposeful movement.
Overall, project results expand our understanding of the areas that form the medial part of parietal association cortex and their respective contributions to sensorimotor behavior. This knowledge has the potential to provide insight regarding the cellular bases of neurological syndromes, including optic ataxia, and to enable future primate studies involving inactivation of specific areas to test clinical hypotheses. Importantly, understanding of the different contributions conveyed by medial parietal areas has the potential to guide accurate placement of prosthetic devices for the control of artificial limbs. This exciting modern field of research aims to assist patients suffering from brain lesions or degenerative disease by restoring a degree of motor abilities.
Research findings have been presented in oral and abstract forms in meetings and in publications in international Peer Reviewed Journals with high impact; one additional publication is currently under revision; further analyses of data for two additional publications are in process after completion of experiments.
It is important to note that experience with this type of methodologies of supervisors Profs. Fattori and Rosa and the Fellow, and close collaboration of the parties and staff at the University of Bologna and Monash University has been pivotal in collecting a large body of high-quality scientific data. An important aspect of the Fellowship, related to its international component, allowed the Fellow to highlight the collaborative nature of the project, particularly via joint presentations of research results to conferences and publications, and via joint co-supervision of students between UniBo and Monash. Equally important, engaging in research in a European and non-European country allowed the Fellow to obtain a broad perspective of current ethical considerations regarding animal studies
Brain circuits involved in the control of reaching and grasping
The cortex located along the medial bank of the intraparietal sulcus has a key role in the integration
of sensory information for accurate reaching and grasping of objects, being fundamental for our
ability to interact with the environment using our arms and hands. Lesions involving this region can
result in optic ataxia, a condition in which people (and other primates) make mistakes when trying to
reach and grasp objects, despite being able to see them. Moreover, damage or disturbances of
neuronal activity in this region lead to other clinically relevant phenomena, such as phantom limbs.
Although it is recognised that the medial intraparietal cortex is likely to encompass more than one
functional area, it remains one of the least well-characterised parts of the primate brain. For example,
physiological studies have proposed the existence of a “parietal reach region” (PRR) in which
neurones encode the locations of objects that will be the target of reaching movements. However, the
extent of the PRR remains unclear, as is its relationship to various functionally distinct areas that
occupy this part of the primate brain.
Building on recent successes in unravelling the organisation of primate sensory association areas
(Rosa et al. 2009; Bakola et al. 2010; Passarelli et al. 2011), this project will achieve the first
integrated view of the neuronal circuitry of the medial intraparietal cortex
Behavioral insights on influence of manual action on object size perception
Visual perception is one of the most advanced function of human brain. The study of different aspects of human perception currently contributes to machine vision applications. Humans estimate the size of objects to grasp them by perceptual mechanisms. However, the motor system is also able to influence the perception system. Here, we found modifications of object size perception after a reaching and a grasping action in different contextual information. This mechanism can be described by the Bayesian model where action provides the likelihood and this latter is integrated with the expected size (prior) derived from the stored object experience (Forward Dynamic Model). Beyond the action-modulation effect, the knowledge of subsequent action type modulates the perceptual responses shaping them according to relevant information required to recognize and interact with objects. Cognitive architectures can be improved on the basis of these processings in order to amplify relevant features of objects and allow to robot/agent an easy interaction with them
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
The human cortical areas V6 and V6A
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
The medial parietal occipital areas in the macaque monkey
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
Parieto-Occipital Sulcus (POS)
Among the areas of the monkey parietal cortex,
those lying inside the parieto-occipital sulcus
(POs), especially in its anterior bank and fundus,
have been of particular interest for neuroscientists
in the last decades. In fact, while the areas in the
posterior bank show simple low-level visual
responses, areas of the anterior bank and on the
fundus have complex high-level visual and
visuomotor functions. In this chapter, we will
describe the main properties of neurons of the
areas located in the POs
Decoding sensorimotor information from superior parietal lobule of macaque via Convolutional Neural Networks
Despite the well-recognized role of the posterior parietal cortex (PPC) in processing sensory information to guide action, the differential encoding properties of this dynamic processing, as operated by different PPC brain areas, are scarcely known. Within the monkey's PPC, the superior parietal lobule hosts areas V6A, PEc, and PE included in the dorso-medial visual stream that is specialized in planning and guiding reaching movements. Here, a Convolutional Neural Network (CNN) approach is used to investigate how the information is processed in these areas. We trained two macaque monkeys to perform a delayed reaching task towards 9 positions (distributed on 3 different depth and direction levels) in the 3D peripersonal space. The activity of single cells was recorded from V6A, PEc, PE and fed to convolutional neural networks that were designed and trained to exploit the temporal structure of neuronal activation patterns, to decode the target positions reached by the monkey. Bayesian Optimization was used to define the main CNN hyper-parameters. In addition to discrete positions in space, we used the same network architecture to decode plausible reaching trajectories. We found that data from the most caudal V6A and PEc areas outperformed PE area in the spatial position decoding. In all areas, decoding accuracies started to increase at the time the target to reach was instructed to the monkey, and reached a plateau at movement onset. The results support a dynamic encoding of the different phases and properties of the reaching movement differentially distributed over a network of interconnected areas. This study highlights the usefulness of neurons' firing rate decoding via CNNs to improve our understanding of how sensorimotor information is encoded in PPC to perform reaching movements. The obtained results may have implications in the perspective of novel neuroprosthetic devices based on the decoding of these rich signals for faithfully carrying out patient's intentions.(C) 2022 Published by Elsevier Ltd
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