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Journal ArticleDOI

Large-Scale Reorganization in the Somatosensory Cortex and Thalamus after Sensory Loss in Macaque Monkeys

22 Oct 2008-The Journal of Neuroscience (Society for Neuroscience)-Vol. 28, Iss: 43, pp 11042-11060
TL;DR: A comparison of the extents of deafferentation across the monkeys shows that even if the dorsal column lesion is partial, preserving most of the hand representation, it is sufficient to induce an expansion of the face representation.
Abstract: Adult brains undergo large-scale plastic changes after peripheral and central injuries. Although it has been shown that both the cortical and thalamic representations can reorganize, uncertainties exist regarding the extent, nature, and time course of changes at each level. We have determined how cortical representations in the somatosensory area 3b and the ventroposterior (VP) nucleus of thalamus are affected by long standing unilateral dorsal column lesions at cervical levels in macaque monkeys. In monkeys with recovery periods of 22-23 months, the intact face inputs expanded into the deafferented hand region of area 3b after complete or partial lesions of the dorsal columns. The expansion of the face region could extend all the way medially into the leg and foot representations. In the same monkeys, similar expansions of the face representation take place in the VP nucleus of the thalamus, indicating that both these processing levels undergo similar reorganizations. The receptive fields of the expanded representations were similar in somatosensory cortex and thalamus. In two monkeys, we determined the extent of the brain reorganization immediately after dorsal column lesions. In these monkeys, the deafferented regions of area 3b and the VP nucleus became unresponsive to the peripheral touch immediately after the lesion. No reorganization was seen in the cortex or the VP nucleus. A comparison of the extents of deafferentation across the monkeys shows that even if the dorsal column lesion is partial, preserving most of the hand representation, it is sufficient to induce an expansion of the face representation.
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Journal ArticleDOI
TL;DR: Brodmann’s area maps were proved to be a useful functional atlas for cortical localization of tactile perception evoked by fabric touch and showed that activation information in the participants’ brain can distinguish the fabric samples very well.
Abstract: Different sensations are generated when we touch textiles with different performance. The mechanical properties related to fabric touch have been studied for a long time, the relationship between which and the subjective feelings is well understood. However, the cognitive mechanism of our brain on the tactile perception evoked by fabric touch were rarely studied. The relationship between mechanical properties of fabrics and the brain response in different areas is the vacancy of the study but urgent problem. In our previous study, the advanced technology of fMRI was proved to be an effective tool for detecting brain response evoked by tactile stimulation of fabric touch with high spatial resolution. Now in this study, further fMRI experiments were conducted to observe brain response when participants touched different fabrics using their fingers in a specified way, and the most widely recognized functional atlas, Brodmann’s area maps, were applied to locate the cortical activations in functional areas. Activations in the participants’s brain in different Brodmann areas was compared with the mechanical preperties of the fabric samples tested by the instruments of KES-FB. The results showed that activation information in the participants’ brain can distinguish the fabric samples very well. Activations in several Brodmann areas are closely connected with different tactile preperties of the fabrics. Therefore, Brodmann’s area maps were proved to be a useful functional atlas for cortical localization of tactile perception evoked by fabric touch.
Journal ArticleDOI
TL;DR: In this article, the authors studied how local circuitries within each layer of the deafferented cortex set the basis for neuroplastic changes after immediate thoracic spinal cord injury (SCI) in anaesthetised rats.
Abstract: Sensory stimulation of forelimb produces cortical evoked responses in the somatosensory hindlimb cortex in a layer-dependent manner Spinal cord injury favours the input statistics of cortico-cortical connections between intact and deafferented cortices After spinal cord injury supragranular layers exhibit better integration of spontaneous of corticocortical information while infragranular layers exhibit better integration of evoked sensory stimulation Cortical reorganization is a layer-specific phenomenon ABSTRACT: Cortical areas have the capacity of large-scale reorganization following sensory deafferentation. However, it remains unclear whether this phenomenon is a unique process that homogenously affects an entire deprived cortical region or it is suitable to changes depending on neuronal networks across distinct cortical layers. Here, we studied how local circuitries within each layer of the deafferented cortex set the basis for neuroplastic changes after immediate thoracic spinal cord injury (SCI) in anaesthetised rats. In vivo electrophysiological recordings from deafferented hindlimb somatosensory cortex showed that SCI induces layer-specific changes mediating evoked and spontaneous activity. In supragranular layers 2/3, SCI increased gamma oscillations and the ability of these neurons to initiate up-states during spontaneous activity, suggesting altered corticocortical network and/or intrinsic properties that may serve to maintain the excitability of the cortical column after deafferentation. On the other hand, SCI enhanced infragranular layers' ability to integrate evoked-sensory inputs leading to increased and faster neuronal responses. Delayed evoked-responses onset were also observed in layers 5/6, suggesting alterations in thalamocortical connectivity. Altogether, our data indicate that SCI immediately modifies local circuitries within the deafferented cortex allowing supragranular layers to better integrate spontaneous corticocortical information, and thus modifying column excitability, and infragranular layers to better integrate evoked-sensory inputs to preserve subcortical outputs. These layer-specific neuronal changes may guide the long-term alterations in neuronal excitability and plasticity associated to the rearrangements of somatosensory networks and the appearance of central sensory pathologies usually associated with spinal cord injury. This article is protected by copyright. All rights reserved.
Journal ArticleDOI
TL;DR: In this article , functional near-infrared spectroscopy (fNIRS) was used to examine the cortical functional differences between individuals with SCI and age-matched healthy controls (HCs), during the performance of stimulus-induced motor tasks and resting-state conditions.
Abstract: Brain reorganization following spinal cord injury (SCI) has been well established using both animal and human studies. Yet, much is unknown regarding the mechanisms associated with positive functional recovery and negative secondary outcomes after SCI. In this study, we use functional near-infrared spectroscopy (fNIRS) to examine the cortical functional differences between individuals with SCI and age-matched healthy controls (HCs), during the performance of stimulus-induced motor tasks and resting-state conditions. We found an overall lower magnitude hemodynamic response curve in the SCI group than the HC group during finger tapping (FT) and finger tapping imagery with action observation (FTI+AO) conditions. We also report overall decreased resting state functional connectivity (RSFC) in the SCI group than HC group; however, significant differences were only found in the Slow-3 frequency range (0.073 to 0.1 Hz). Lastly, upon correlating task-based FC and RSFC with the duration of injury in the SCI group, we found that a longer injury duration was significantly associated with lower task-based FC within the medial sensorimotor network (mSMN) during the FT task condition. However, we found no significant association between RSFC and the duration of injury in individuals with SCI. These results provide insight regarding the use of fNIRS in rehabilitative therapies for individuals with SCI and allow for a better understanding of cortical functional alterations after SCI.
Journal ArticleDOI
TL;DR: In this paper , the extent of the deafferentation and the duration of the recovery period are two major factors that determine the extent and extent of reorganization of the cuneate nucleus in the medulla.
Abstract: Spinal cord injury is a devastating condition that haunts human lives. Typically, patients experience referred phantom sensations on the hand when they are touched on the face. In adult monkeys, massive deafferentations such as chronic dorsal column lesions at higher cervical levels result in the large-scale expansion of face inputs into the deafferented hand cortex of area 3b. However, adult rats with thoracic dorsal column lesions do not demonstrate such large-scale reorganization. The large-scale face expansion in area 3b of monkeys is driven by the reorganization of the cuneate nucleus in the medulla. The sprouting of afferents from the trigeminal nucleus to the adjacent deafferented cuneate nucleus is facilitated by close proximity and compactness of the medulla in primates. Previously, in adult rats with thoracic lesions, the cuneate nucleus was not deafferented and its functional organization was not explored. The extent of the deafferentation and the duration of the recovery period are two major factors that determine the extent of reorganization. Hence, higher cervical (C3-C4) dorsal column lesions were performed, which cause massive deafferentations, and physiological maps were obtained after prolonged recovery periods (3 weeks -18 months). In spite of the above, the expansion of the intact face inputs was not observed in the deafferented zones of the primary somatosensory cortex (SI) and medulla of adult rats. The deafferented forelimb and hindlimb representations in SI were unresponsive to cutaneous stimulation of any part of the body. The cuneate and gracile nuclei in rats with complete dorsal column lesions remained mostly inactive except for a few sites which responded to stimulation of the spared upper arm. Hence, dorsal column lesions have different effects on the adult primate and rodent somatosensory systems. Appreciating this inter-species difference can aid in identifying the underlying neural substrates and restrict maladaptive reorganizations to cure phantom sensations.
Posted ContentDOI
11 Feb 2020-bioRxiv
TL;DR: Comparing visual maps in the brains of early deaf and hearing adults is found to find a redistribution of neural resources in the lateral geniculate nucleus and primary visual cortex, with larger representations of the periphery, at a cost of smaller representation of the central visual field.
Abstract: Deaf individuals rely on visual rather than auditory cues to detect events in the periphery, putting a greater demand on neural resources for vision. Comparing visual maps in the brains of early deaf and hearing adults, we found a redistribution of neural resources in the lateral geniculate nucleus and primary visual cortex, with larger representations of the periphery, at a cost of smaller representations of the central visual field.

Cites background from "Large-Scale Reorganization in the S..."

  • ...Parallel studies in the somatosensory system also indicate that thalamic projections can influence cortical plasticity further along the processing pathway (Jain et al., 2008)....

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References
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Journal ArticleDOI
TL;DR: The results indicated that the deprivation caused by monocular suture produced a decrease in the cytochrome oxidase staining of the binocular segment of the deprived geniculate laminae of kittens, leading to a significant decreases in the level of oxidative enzyme activity one to several synapses away.

1,862 citations

Journal ArticleDOI
08 Jun 1995-Nature
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


"Large-Scale Reorganization in the S..." refers background in this paper

  • ...A small expansion of the face inputs into the hand region of the cortex was seen long after hand or arm amputations (Flor et al., 1995; Florence and Kaas, 1995; Grüsser et al., 2004), or immediately after median and radial nerve injury or block (Silva et al....

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Journal ArticleDOI
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


"Large-Scale Reorganization in the S..." refers background in this paper

  • ...…the cortical maps has been demonstrated in a variety of mammalian species after different kinds of deprivations including digit or limb amputations (Merzenich et al., 1984; Wall and Cusick, 1984; Calford and Tweedale, 1988; Turnbull and Rasmusson, 1991; Florence et al., 1998), nerve transections…...

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  • ...Since then, reorganization of the cortical maps has been demonstrated in a variety of mammalian species after different kinds of deprivations including digit or limb amputations (Merzenich et al., 1984; Wall and Cusick, 1984; Calford and Tweedale, 1988; Turnbull and Rasmusson, 1991; Florence et al., 1998), nerve transections (Wall and Kaas, 1985; Garraghty and Kaas, 1991b), dorsal root transections (Pons et al....

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Journal ArticleDOI
28 Jun 1991-Science
TL;DR: The results show the need for a reevaluation of both the upper limit of cortical reorganization in adult primates and the mechanisms responsible for it.
Abstract: After limited sensory deafferentations in adult primates, somatosensory cortical maps reorganize over a distance of 1 to 2 millimeters mediolaterally, that is, in the dimension along which different body parts are represented. This amount of reorganization was considered to be an upper limit imposed by the size of the projection zones of individual thalamocortical axons, which typically also extend a mediolateral distance of 1 to 2 millimeters. However, after extensive long-term deafferentations in adult primates, changes in cortical maps were found to be an order of magnitude greater than those previously described. These results show the need for a reevaluation of both the upper limit of cortical reorganization in adult primates and the mechanisms responsible for it.

1,051 citations


"Large-Scale Reorganization in the S..." refers background or methods in this paper

  • ...It is possible that this has not been reported before because the foot region of the cortex was not mapped previously (Pons et al., 1991; Jain et al., 1997)....

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  • ...in macaque monkeys (Pons et al., 1991) and a comparable 5 mm...

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  • ...After an extensive recovery period the boundaries of the face representation shift medially into the hand region by as much as 10 –14 mm in macaque monkeys (Pons et al., 1991) and a comparable 5 mm in smaller owl monkeys (Jain et al., 1997)....

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  • ...Limits of plasticity in area 3b The maximal extent of shift in representational boundaries reported before this study is in the range of 10 –14 mm for macaque monkeys (Pons et al., 1991) and 5 mm for smaller brained owl monkeys (Jain et al....

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  • ...In contrast, after transection of the dorsal roots of the spinal cord from C2 to T4, the deprived hand, arm, and occiput regions of area 3b come to respond to the inputs from the chin (Pons et al., 1991)....

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Journal ArticleDOI
TL;DR: This paper found that after the median nerve was transected and ligated in adult owl and squirrel monkeys, the cortical sectors representing it within skin surface representations in Areas 3b and 1 were completely occupied by 'new' and expanded representations of surrounding skin fields.

948 citations