Stability of Sensory Topographies in Adult Cortex
TL;DR: It is concluded that the cortical representation of the limb remains remarkably stable despite the loss of its main peripheral input and the implications of the stability of sensory representations on the development of upper-limb neuroprostheses.
About: This article is published in Trends in Cognitive Sciences.The article was published on 2017-03-01 and is currently open access. It has received 109 citations till now. The article focuses on the topics: Sensory maps and brain development & Sensory neuroscience.
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TL;DR: The present work overviews the current reports dealing with the several features that can be used to improve peripheral nerve regeneration (PNR), ranging from the simple use of hollow NGCs to tissue engineered intraluminal fillers, or to even more advanced strategies, comprising the molecular and gene therapies as well as cell-based therapies.
Abstract: Peripheral nerve repair and regeneration remains among the greatest challenges in tissue engineering and regenerative medicine. Even though peripheral nerve injuries (PNIs) are capable of some degree of regeneration, frail recovery is seen even when the best microsurgical technique is applied. PNIs are known to be very incapacitating for the patient, due to the deprivation of motor and sensory abilities. Since there is no optimal solution for tackling this problem up to this day, the evolution in the field is constant, with innovative designs of advanced nerve guidance conduits (NGCs) being reported every day. As a basic concept, a NGC should act as a physical barrier from the external environment, concomitantly acting as physical guidance for the regenerative axons across the gap lesion. NGCs should also be able to retain the naturally released nerve growth factors secreted by the damaged nerve stumps, as well as reducing the invasion of scar tissue-forming fibroblasts to the injury site. Based on the neurobiological knowledge related to the events that succeed after a nerve injury, neuronal subsistence is subjected to the existence of an ideal environment of growth factors, hormones, cytokines, and extracellular matrix (ECM) factors. Therefore, it is known that multifunctional NGCs fabricated through combinatorial approaches are needed to improve the functional and clinical outcomes after PNIs. The present work overviews the current reports dealing with the several features that can be used to improve peripheral nerve regeneration (PNR), ranging from the simple use of hollow NGCs to tissue engineered intraluminal fillers, or to even more advanced strategies, comprising the molecular and gene therapies as well as cell-based therapies.
160 citations
TL;DR: This work has shown that an effective hand replacement can be achieved if the user, in addition to motor functions, is provided with the sensations that are naturally perceived while grasping and moving.
Abstract: OBJECTIVE Hand amputation is a highly disabling event, which significantly affects quality of life. An effective hand replacement can be achieved if the user, in addition to motor functions, is provided with the sensations that are naturally perceived while grasping and moving. Intraneural peripheral electrodes have shown promising results toward the restoration of the sense of touch. However, the long-term usability and clinical relevance of intraneural sensory feedback have not yet been clearly demonstrated. METHODS To this aim, we performed a 6-month clinical study with 3 transradial amputees who received implants of transverse intrafascicular multichannel electrodes (TIMEs) in their median and ulnar nerves. After calibration, electrical stimulation was delivered through the TIMEs connected to artificial sensors in the digits of a prosthesis to generate sensory feedback, which was then used by the subjects while performing different grasping tasks. RESULTS All subjects, notwithstanding their important clinical differences, reported stimulation-induced sensations from the phantom hand for the whole duration of the trial. They also successfully integrated the sensory feedback into their motor control strategies while performing experimental tests simulating tasks of real life (with and without the support of vision). Finally, they reported a decrement of their phantom limb pain and a general improvement in mood state. INTERPRETATION The promising results achieved with all subjects show the feasibility of the use of intraneural stimulation in clinical settings. ANN NEUROL 2019;85:137-154.
127 citations
Cites background from "Stability of Sensory Topographies i..."
...Another possibility (not excluding the previous one) is that the continuous stimulation of peripheral nerves (generating a peculiar pattern of sensation) combined with the intensive use of the prosthetic hand may have promoted a process of embodiment of the device (taking advantage of brain plasticity), with a progressive association of the peculiar pattern of sensations with the prosthetic hand itself.(50) Because the clinical features of ALM and LRP were very different, we hypothesize that this phenomenon...
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TL;DR: Non-invasive and invasive technologies for conveying artificial sensory feedback through bionic hands are described, and the technologies' long-term prospects are evaluated.
Abstract: Individuals who have lost the use of their hands because of amputation or spinal cord injury can use prosthetic hands to restore their independence. A dexterous prosthesis requires the acquisition of control signals that drive the movements of the robotic hand, and the transmission of sensory signals to convey information to the user about the consequences of these movements. In this Review, we describe non-invasive and invasive technologies for conveying artificial sensory feedback through bionic hands, and evaluate the technologies’ long-term prospects. This Review discusses non-invasive and invasive technologies for conveying artificial sensory feedback through bionic hands.
95 citations
TL;DR: It is concluded that back pain-induced disrupted or reduced proprioceptive signaling likely plays a pivotal role in driving long-term changes in the top-down control of the motor system via motor and sensory cortical reorganization.
Abstract: Motor control, which relies on constant communication between motor and sensory systems, is crucial for spine posture, stability and movement. Adaptions of motor control occur in low back pain (LBP) while different motor adaption strategies exist across individuals, probably to reduce LBP and risk of injury. However, in some individuals with LBP, adapted motor control strategies might have long-term consequences, such as increased spinal loading that has been linked with degeneration of intervertebral discs and other tissues, potentially maintaining recurrent or chronic LBP. Factors contributing to motor control adaptations in LBP have been extensively studied on the motor output side, but less attention has been paid to changes in sensory input, specifically proprioception. Furthermore, motor cortex reorganization has been linked with chronic and recurrent LBP, but underlying factors are poorly understood. Here, we review current research on behavioral and neural effects of motor control adaptions in LBP. We conclude that back pain-induced disrupted or reduced proprioceptive signaling likely plays a pivotal role in driving long-term changes in the top-down control of the motor system via motor and sensory cortical reorganization. In the outlook of this review, we explore whether motor control adaptations are also important for other (musculoskeletal) pain conditions.
72 citations
Cites background from "Stability of Sensory Topographies i..."
...Therefore, systematic cortical mapping of paraspinal proprioceptive input will be essential for a better understanding of its role in aberrant sensorimotor integration and related potential maladaptive cortical plasticity in chronic LBP (Makin and Bensmaia 2017; Massé-Alarie and Schneider 2016)....
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TL;DR: It was found that compensatory behaviors in one-handers involved multiple body parts (residual arm, lips, and feet), and this diversified compensatory profile was associated with large-scale cortical reorganization, regardless of cortical proximity to the hand territory.
69 citations
Cites background from "Stability of Sensory Topographies i..."
...For example, the unmasking of otherwise-silenced connections may not necessarily be harnessed to guide behavior [31]....
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References
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TL;DR: In this paper, the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI data from 1,000 subjects and a clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex.
Abstract: Information processing in the cerebral cortex involves interactions among distributed areas. Anatomical connectivity suggests that certain areas form local hierarchical relations such as within the visual system. Other connectivity patterns, particularly among association areas, suggest the presence of large-scale circuits without clear hierarchical relations. In this study the organization of networks in the human cerebrum was explored using resting-state functional connectivity MRI. Data from 1,000 subjects were registered using surface-based alignment. A clustering approach was employed to identify and replicate networks of functionally coupled regions across the cerebral cortex. The results revealed local networks confined to sensory and motor cortices as well as distributed networks of association regions. Within the sensory and motor cortices, functional connectivity followed topographic representations across adjacent areas. In association cortex, the connectivity patterns often showed abrupt transitions between network boundaries. Focused analyses were performed to better understand properties of network connectivity. A canonical sensory-motor pathway involving primary visual area, putative middle temporal area complex (MT+), lateral intraparietal area, and frontal eye field was analyzed to explore how interactions might arise within and between networks. Results showed that adjacent regions of the MT+ complex demonstrate differential connectivity consistent with a hierarchical pathway that spans networks. The functional connectivity of parietal and prefrontal association cortices was next explored. Distinct connectivity profiles of neighboring regions suggest they participate in distributed networks that, while showing evidence for interactions, are embedded within largely parallel, interdigitated circuits. We conclude by discussing the organization of these large-scale cerebral networks in relation to monkey anatomy and their potential evolutionary expansion in humans to support cognition.
6,284 citations
TL;DR: Using multi-modal magnetic resonance images from the Human Connectome Project and an objective semi-automated neuroanatomical approach, 180 areas per hemisphere are delineated bounded by sharp changes in cortical architecture, function, connectivity, and/or topography in a precisely aligned group average of 210 healthy young adults.
Abstract: Understanding the amazingly complex human cerebral cortex requires a map (or parcellation) of its major subdivisions, known as cortical areas. Making an accurate areal map has been a century-old objective in neuroscience. Using multi-modal magnetic resonance images from the Human Connectome Project (HCP) and an objective semi-automated neuroanatomical approach, we delineated 180 areas per hemisphere bounded by sharp changes in cortical architecture, function, connectivity, and/or topography in a precisely aligned group average of 210 healthy young adults. We characterized 97 new areas and 83 areas previously reported using post-mortem microscopy or other specialized study-specific approaches. To enable automated delineation and identification of these areas in new HCP subjects and in future studies, we trained a machine-learning classifier to recognize the multi-modal 'fingerprint' of each cortical area. This classifier detected the presence of 96.6% of the cortical areas in new subjects, replicated the group parcellation, and could correctly locate areas in individuals with atypical parcellations. The freely available parcellation and classifier will enable substantially improved neuroanatomical precision for studies of the structural and functional organization of human cerebral cortex and its variation across individuals and in development, aging, and disease.
3,414 citations
TL;DR: A very strong direct relationship is reported between the amount of cortical reorganization and the magnitude of phantom limb pain (but not non-painful phantom phenomena) experienced after arm amputation, indicating that phantom-limb pain is related to, and may be a consequence of, plastic changes in primary somatosensory cortex.
Abstract: Although phantom-limb pain is a frequent consequence of the amputation of an extremity, little is known about its origin. On the basis of the demonstration of substantial plasticity of the somatosensory cortex after amputation or somatosensory deafferentation in adult monkeys, it has been suggested that cortical reorganization could account for some non-painful phantom-limb phenomena in amputees and that cortical reorganization has an adaptive (that is, pain-preventing) function. Theoretical and empirical work on chronic back pain has revealed a positive relationship between the amount of cortical alteration and the magnitude of pain, so we predicted that cortical reorganization and phantom-limb pain should be positively related. Using non-invasive neuromagnetic imaging techniques to determine cortical reorganization in humans, we report a very strong direct relationship (r = 0.93) between the amount of cortical reorganization and the magnitude of phantom limb pain (but not non-painful phantom phenomena) experienced after arm amputation. These data indicate that phantom-limb pain is related to, and may be a consequence of, plastic changes in primary somatosensory cortex.
1,692 citations
TL;DR: In these experiments the use of monocular deprivation made it possible to compare adjacent geniculate layers, and also to compare the two eyes in their ability to influence cortical cells, so that each animal acted, in a sense, as its own control.
Abstract: IN THE NORMAL CAT OR KITTEN about four-fifths of cells in the striate cortex can be driven by both eyes (3, 4). If, however, one eye of a newborn kitten is sewn shut and the visual cortex recorded from 3 months later, only a small fraction of cells can be driven from the deprived eye (8) . In contrast, many cells in the latera .I geniculate are driven normally from the d ,eprived eye (7 ), suggesting that the abnormality occurs somewhere between geniculate cells and cortex. Since clear receptive-field orientations and directional preferences to movement are seen in cortical cells of newborn visually inexperienced kittens, the deprivation effects presumably represent some sort of disruption of innately determined connections, rather than a failure of postnatal development related to lack of experience. In these experiments the use of monocular deprivation made it possible to compare adjacent geniculate layers, and also to compare the two eyes in their ability to influence cortical cells, so that each animal acted, in a sense, as its own control. The results led us to expect that depriving both eyes for similar periods would lead to an almost total unresponsiveness of cortical cells to stimulation of either eye. That should be so, provided the effects of depriving one eye were independent of whether or not the other eye was simultaneously deprived. It seemed worthwhile to test such an assumption, since any interdependence of the two pathways would be of considerable interest. We accordingly raised kittens with both eyes covered by lid suture, and recorded from the striate cortex when the animals had reached an age of 23-43 months.
1,520 citations
TL;DR: The cortical representations of the hand in area 3b in adult owl monkeys were defined with use of microelectrode mapping techniques 2–8 months after surgical amputation of digit 3, or of both digits 2 and 3.
Abstract: The cortical representations ofthe hand in area 3b in adult owl monkeys were defined with use of microelectrode mapping techniques 2-8 months after surgical amputation of digit 3, or of both digits 2 and 3. Digital nerves were tied to prevent their regeneration within the amputation stump. Suc cessive maps were derived in several monkeys to determine the nature of changes in map organization in the same individuals over time. In all monkeys studied, the representations of adjacent digits and pal mar surfaces expanded topographically to occupy most or all of the cortical territories formerly representing the amputated digit(s). With the expansion of the representations of these surrounding skin surfaces (1) there were severalfold increases in their magnification and (2) roughly corresponding decreases in receptive field areas. Thus, with increases in magnification, surrounding skin surfaces were represented in correspondingly finer grain, implying that the rule relating receptive field overlap to separation in distance across the cortex (see Sur et aI., '80) was dynamically maintained as receptive fields progressively decreased in size. These studies also revealed that: (1) the discontinuities between the representations of the digits underwent significant translocations (usually by hundreds of microns) after amputation, and sharp new discontinuous boundaries formed where usually separated, expanded digital representa tions (e.g., of digits 1 and 4) approached each other in the reorganizing map, implying that these map discontinuities are normally dynamically main tained. (2) Changes in receptive field sizes with expansion of representations of surrounding skin surfaces into the deprived cortical zone had a spatial distribution and time course similar to changes in sensory acuity on the stumps of human amputees. This suggests that experience-dependent map changes result in changes in sensory capabilities. (3) The major topographic changes were limited to a cortical zone 500-700 JIm on either side of the initial boundaries of the representation of the amputated digits. More dis tant regions did not appear to reorganize (i.e., were not occupied by inputs from surrounding skin surfaces) even many months after amputation. (4) The representations of some skin surfaces moved in entirety to locations within the former territories of representation of amputated digits in every
1,327 citations
"Stability of Sensory Topographies i..." refers background in this paper
...For example, SI remapping following digit amputation results in increased representation of the neighbouring digits, which in turn should lead to increased acuity for these digits [8]....
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...Removal of input from a body part (due to amputation [8] or nerve transection [9]) results in changes in the somatotopic organisation, such that the representation of cortically adjacent body parts seems to take over the ‘freed up’ brain territory (see [10] for a review of...
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