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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.
Citations
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Journal ArticleDOI
TL;DR: The neuroplasticity of the brain and spinal cord after spinal Cord injury in rats, non-human primates, and humans is discussed and a brief overview of emerging interventions to induce plasticity in humans with spinal cord injury will be discussed.

46 citations

Journal ArticleDOI
TL;DR: The current state of research in regard to the demographics, causal factors, and treatments of phantom limb pain is described, based on an increasing body of research on neurophysiological changes after amputation.
Abstract: Phantom sensations, that is, sensations perceived in a body part that has been lost, are a common consequence of accidental or clinical extremity amputations. Most amputation patients report a continuing presence of the limb, with some describing additional sensations such as numbness, tickling, or cramping of the phantom limb. The type, frequency, and stability of these phantom sensations can vary immensely. The phenomenon of painful phantom sensations, that is, phantom limb pain, presents a challenge for practitioners and researchers and is often detrimental to the patient's quality of life. In addition to the use of conventional therapies for chronic pain disorders, recent years have seen the development of novel treatments for phantom limb pain, based on an increasing body of research on neurophysiological changes after amputation. This article describes the current state of research in regard to the demographics, causal factors, and treatments of phantom limb pain.

46 citations

Journal ArticleDOI
TL;DR: The results show that exercise not only increased the percentage of responding cells in the hindlimb SI but also increased the magnitude of the response of these cells, and this increase in response magnitude was correlated with behavioral outcome measures.
Abstract: Exercise-induced cortical plasticity is associated with improved functional outcome after brain or nerve injury. Exercise also improves functional outcomes after spinal cord injury, but its effects on cortical plasticity are not known. The goal of this investigation was to study the effect of moderate exercise (treadmill locomotion, 3 min/d, 5 d/week) on the somatotopic organization of forelimb and hindlimb somatosensory cortex (SI) after neonatal thoracic transection. We used adult rats spinalized as neonates because some of these animals develop weight-supported stepping, and, therefore, the relationship between cortical plasticity and stepping could also be examined. Acute, single-neuron mapping was used to determine the percentage of cortical cells responding to cutaneous forelimb stimulation in normal, spinalized, and exercised spinalized rats. Multiple single-neuron recording from arrays of chronically implanted microwires examined the magnitude of response of these cells in normal and exercised spinalized rats. Our results show that exercise not only increased the percentage of responding cells in the hindlimb SI but also increased the magnitude of the response of these cells. This increase in response magnitude was correlated with behavioral outcome measures. In the forelimb SI, neonatal transection reduced the percentage of responding cells to forelimb stimulation, but exercise reversed this loss. This restoration in the percentage of responding cells after exercise was accompanied by an increase in their response magnitude. Therefore, the increase in responsiveness of hindlimb SI to forelimb stimulation after neonatal transection and exercise may be due, in part, to the effect of exercise on the forelimb SI.

46 citations


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

  • ...However, a recent study in primate using a unilateral cervical spinal cord injury demonstrated reorganization in the thalamus that paralleled that of the cortex after 2 years (Jain et al., 2008)....

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Journal ArticleDOI
TL;DR: The observations suggest that subthreshold activity plays an important role in the reactivation of deafferented cortex and could promote behavioral recovery and reveals differences between functional imaging and microelectrode recording maps.
Abstract: Somatosensory cortices of adult primates reactivate over time after sensory loss. The time course and the neural mechanisms underlying the cortical reactivation are not well understood. Here we report that longitudinal high-resolution functional magnetic resonance imaging (fMRI) studies on anesthetized squirrel monkeys revealed dynamic reorganizations of digit activations in area 3b, within 2 months after severely disrupting afferent inputs by dorsal column section. We found that digit regions in which inputs were severely disrupted exhibited fMRI tactile responses. Reorganization was characterized by an early moving away phase and a late returning phase, as indicated by spatial shifts of individual digit activation centers in relation to the pre-lesion activation sites. Subsequent optical imaging studies confirmed fMRI activations, and dense microelectrode penetrations identified weak neuronal activity at the reactivated sites. Activation zones detected by fMRI and optical imaging were significantly larger in input-deprived than normal input single-digit regions and were larger than regions defined by neuronal spiking activity. This study captures the dynamic reorganization of digit representations after dorsal column lesions and reveals differences between functional imaging and microelectrode recording maps. Our observations suggest that subthreshold activity plays an important role in the reactivation of deafferented cortex and could promote behavioral recovery.

44 citations


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

  • ...…Darian-Smith and Ciferri, 2006; Kaas et al., 2008; Qi et al., 2011) and has shown that the reactivation of area 3b, along with other cortical and subcortical regions (Jain et al., 1997, 2008), contribute significantly to the functional and behavioral recovery of the damaged sensorimotor functions....

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  • ...Although the neuronal response properties characterized at the end of the 2–3 months recovery period are similar to previous findings (Jain et al., 1997, 1998, 2008), we identified here a dynamic shift of individual digit activation centers during this recovery period....

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  • ...…(Flor et al., 1995, 1997; Mühlnickel et al., 1998; Karl et al., 2001; Muellbacher and Hallett, 2006; Fox 2009), although the neuronal mechanisms underlying plastic changes in the brain and behavioral recoveries remain unclear (for discussion, see Jain et al., 2008; Graziano and Jones, 2009)....

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  • ...Additional details about surgical procedures can be found in previous publications from the laboratory (Jain et al., 1997, 2008; Qi et al., 2011)....

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Journal ArticleDOI
TL;DR: The results are consistent with the proposal that the treatment enhances the sprouting of digit 1 afferents in the cuneate nucleus and that this sprouting allowed these preserved inputs to activate cortex more effectively.
Abstract: After large but incomplete lesions of ascending dorsal column afferents in the cervical spinal cord, the hand representation in the contralateral primary somatosensory cortex (area 3b) of monkeys is largely or completely unresponsive to touch on the hand. However, after weeks of spontaneous recovery, considerable reactivation of the hand territory in area 3b can occur. Because the reactivation process likely depends on the sprouting of remaining axons from the hand in the cuneate nucleus of the lower brainstem, we sought to influence cortical reactivation by treating the cuneate nucleus with an enzyme, chondroitinase ABC, that digests perineuronal nets, promoting axon sprouting. Dorsal column lesions were placed at a spinal cord level (C5/C6) that allowed a portion of ascending afferents from digit 1 to survive in squirrel monkeys. After 11–12 wk of recovery, the contralateral forelimb cortex was reactivated by stimulating digit 1 more extensively in treated monkeys than in control monkeys. The results are consistent with the proposal that the treatment enhances the sprouting of digit 1 afferents in the cuneate nucleus and that this sprouting allowed these preserved inputs to activate cortex more effectively.

41 citations


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

  • ...Similar results have been reported in other studies of monkeys after dorsal column lesions (2, 4, 5)....

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  • ...When somatosensory inputs from the hand have been largely removed in monkeys by cutting ascending branches of cutaneous afferents in the dorsal column pathways of the spinal cord (2, 4, 5) or by selectively cutting the dorsal roots of peripheral nerves subserving a part of the hand (3), most of the territory of the representation of the hand in the contralateral primary somatosensory cortex (area 3b) initially fails to respond to touch on the hand....

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  • ...The existence of both unresponsive sites and sites responsive to various locations on the hand have been reported in previous studies of the effects of spontaneous reactivation of hand cortex after dorsal column lesions in monkeys (2, 4, 5)....

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References
More filters
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