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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 results demonstrate that peripheral inputs from both extremities overlap on neuronal populations in the somatosensory thalamus and show that the responses of thalamic neurons to forepaw and hindpaw stimuli are increased immediately after SCI, in association with a specific decrease in spontaneous activity in the hindpawed locations.

34 citations


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

  • ...But only few studies focused on thalamic spontaneous activity as well as the evoked responses that are expanded into the thalamic deafferented region (Gerke et al., 2003; Jain et al., 2008; Liang and Mendell, 2013)....

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Journal ArticleDOI
TL;DR: Evidence is sought of cortical reorganization and related sensory and motor improvements following pharmacologically induced TFD of the stroke-affected forearm, accompanied by cortical plasticity, which might improve the somatosensory and motor functions of the Stroke-affected upper limb.
Abstract: Following stroke, many patients suffer from chronic motor impairment and reduced somatosensation in the stroke-affected body parts. Recent experimental studies suggest that temporary functional deafferentation (TFD) of parts of the stroke-affected upper limb or of the less-affected contralateral limb might improve the sensorimotor capacity of the stroke-affected hand. The present study sought evidence of cortical reorganization and related sensory and motor improvements following pharmacologically induced TFD of the stroke-affected forearm. Examination was performed during 2 d of Constraint-Induced Movement Therapy. Thirty-six human patients were deafferented on the stroke-affected forearm by an anesthetic cream (containing lidocaine and prilocaine) on one of the 2 d, and a placebo cream was applied on the other. The order of TFD and placebo treatment was counterbalanced across patients. Somatosensory and motor performance were assessed using a Grating orienting task and a Shape-sorter-drum task, and with somatosensory-evoked magnetic fields. Evoked magnetic fields showed significant pre- to postevaluation magnitude increases in response to tactile stimulation of the thumb of the stroke-affected hand during TFD but not following placebo treatment. We also observed a rapid extension of the distance between cortical representations of the stroke-affected thumb and little finger following TFD but not following placebo treatment. Moreover, somatosensory and motor performance of the stroke-affected hand was significantly enhanced during TFD but not during placebo treatment. Thus, pharmacologically induced TFD of a stroke-affected forearm might improve the somatosensory and motor functions of the stroke-affected upper limb, accompanied by cortical plasticity.

34 citations


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

  • ...…above, the observed improvements are probably based on rapid changes in the receptive fields at different levels of the somatosensory system, e.g., in the somatosensory cortex as well as in the thalamus (Nicolelis et al., 1993; Weiss et al., 2004; Jain et al., 2008; Björkman et al., 2009)....

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  • ..., in the somatosensory cortex as well as in the thalamus (Nicolelis et al., 1993; Weiss et al., 2004; Jain et al., 2008; Björkman et al., 2009)....

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Journal ArticleDOI
TL;DR: The results suggest that rTMS therapy beginning in the acute phase after SCI promotes neuroplasticity and is an effective rehabilitative approach in a rat model of SCI.
Abstract: Introduction: Spinal cord injury (SCI) causes partial or complete damage to sensory and motor pathways and induces immediate changes in cortical function. Current rehabilitative strategies do not address this early alteration, therefore impacting the degree of neuroplasticity and subsequent recovery. The following study aims to test if a non-invasive brain stimulation technique such as repetitive transcranial magnetic stimulation (rTMS) is effective in promoting plasticity and rehabilitation, and can be used as an early intervention strategy in a rat model of SCI. Methods: A contusion SCI was induced at segment T9 in adult rats. An rTMS coil was positioned over the brain to deliver high frequency stimulation. Behavior, motor and sensory functions were tested in three groups: SCI rats that received high-frequency (20 Hz) rTMS within 10 min post-injury (acute-TMS; n = 7); SCI rats that received TMS starting 2 weeks post-injury (chronic-TMS; n = 5), and SCI rats that received sham TMS (no-TMS, n = 5). Locomotion was evaluated by the Basso, Beattie, and Bresnahan (BBB) and gridwalk tests. Motor evoked potentials (MEP) were recorded from the forepaw across all groups to measure integrity of motor pathways. Functional MRI (fMRI) responses to contralateral tactile hindlimb stimulation were measured in an 11.7T horizontal bore small-animal scanner. Results: The acute-TMS group demonstrated the fastest improvements in locomotor performance in both the BBB and gridwalk tests compared to chronic and no-TMS groups. MEP responses from forepaw showed significantly greater difference in the inter-peak latency between acute-TMS and no-TMS groups, suggesting increases in motor function. Finally, the acute-TMS group showed increased fMRI-evoked responses to hindlimb stimulation over the right and left hindlimb (LHL) primary somatosensory representations (S1), respectively; the chronic-TMS group showed moderate sensory responses in comparison, and the no-TMS group exhibited the lowest sensory responses to both hindlimbs. Conclusion: The results suggest that rTMS therapy beginning in the acute phase after SCI promotes neuroplasticity and is an effective rehabilitative approach in a rat model of SCI.

33 citations

Journal ArticleDOI
TL;DR: Slow, inexorable progression of lemniscal and thalamocortical axonal withdrawal is a neurodegenerative phenomenon likely to be a powerful inducement to compensatory long-term plasticity, a mechanism that can explain the long- term evolution of cortical reorganization and, with it, phantom sensations in spinal patients and amputees.
Abstract: The mechanisms responsible for long-term, massive reorganization of representational maps in primate somatosensory cortex after deafferentation are poorly understood. Sprouting of cortical axons cannot account for the extent of reorganization, and withdrawal of axons of deafferented brainstem and thalamic neurons, permitting expression of previously silent synapses, has not been directly demonstrated. This study is focused on the second of these. In monkeys, deafferented for two years by section of the cuneate fasciculus at the C1 level, there was extensive withdrawal of axon terminals from thalamus and cortex, detectable a decade before visible atrophy of their parent neuronal somata in the cuneate nucleus or thalamus. Slow, inexorable progression of lemniscal and thalamocortical axonal withdrawal is a neurodegenerative phenomenon likely to be a powerful inducement to compensatory long-term plasticity, a mechanism that can explain the long-term evolution of cortical reorganization and, with it, phantom sensations in spinal patients and amputees.

33 citations


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

  • ...Other studies reported massive expansion of the cortical face representation after lesion of the dorsal columns at levels varying from C3 to C7 (Jain et al., 1997; Jain et al., 2008)....

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  • ...Two years after a spinal injury of this type, no clear cellular atrophy has been reported in the brainstem or thalamus (Cowan et al., 1970), and that was confirmed in the present study, but cortical reorganization is demonstrable (Merzenich et al., 1984; Jain et al., 2008)....

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  • ..., 1970), and that was confirmed in the present study, but cortical reorganization is demonstrable (Merzenich et al., 1984; Jain et al., 2008)....

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Journal ArticleDOI
TL;DR: It is concluded that preserved dorsal column afferents after nearly complete lesions contribute to the reactivation of cortex and the recovery of the behavior, but second-order sensory pathways in the spinal cord may also play an important role.
Abstract: In our experiments, we removed a major source of activation of somatosensory cortex in mature monkeys by unilaterally sectioning the sensory afferents in the dorsal columns of the spinal cord at a high cervical level. At this level, the ascending branches of tactile afferents from the hand are cut, while other branches of these afferents remain intact to terminate on neurons in the dorsal horn of the spinal cord. Immediately after such a lesion, the monkeys seem relatively unimpaired in locomotion and often use the forelimb, but further inspection reveals that they prefer to use the unaffected hand in reaching for food. In addition, systematic testing indicates that they make more errors in retrieving pieces of food, and start using visual inspection of the rotated hand to confirm the success of the grasping of the food. Such difficulties are not surprising as a complete dorsal column lesion totally deactivates the contralateral hand representation in primary somatosensory cortex (area 3b). However, hand use rapidly improves over the first post-lesion weeks, and much of the hand representational territory in contralateral area 3b is reactivated by inputs from the hand in roughly a normal somatotopic pattern. Quantitative measures of single neuron response properties reveal that reactivated neurons respond to tactile stimulation on the hand with high firing rates and only slightly longer latencies. We conclude that preserved dorsal column afferents after nearly complete lesions contribute to the reactivation of cortex and the recovery of the behavior, but second-order sensory pathways in the spinal cord may also play an important role. Our microelectrode recordings indicate that these preserved first-order, and second-order pathways are initially weak and largely ineffective in activating cortex, but they are potentiated during the recovery process. Therapies that would promote this potentiation could usefully enhance recovery after spinal cord injury.

32 citations


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

  • ...…al., 1997; Florence et al., 1998; Li et al., 2013), the section of peripheral nerve afferents as they travel in the dorsal columns of spinal cord (Jain et al., 1997, 1998, 2000, 2008; Weng et al., 2003; Graziano and Jones, 2009; Qi et al., 2011a), or spinal cord injury in rodents (Ghosh et al.,…...

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  • ...We and others have also studied area 3b reorganization in macaque monkey (Pons et al., 1991; Florence and Kaas, 1995; Florence et al., 1998; Darian-Smith and Brown, 2000; Jain et al., 2008), where area 3b is hidden on the caudal bank of a deep central fissure, as in humans....

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  • ...Such results have been reported in a number of studies, including those from owl monkeys, squirrel monkeys, marmosets, and macaque monkeys (Jain et al., 1997, 1998, 2008; Qi et al., 2011a; Bowes et al., 2012, 2013)....

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  • ...…the area 1 representation of touch is restored in a somatotopic pattern that generally parallels that in area 3b, but it is less precise in detailed somatotopy, and the neuronal responses tend to be weaker in the reactivated regions (Merzenich et al., 1983a; Jain et al., 2008; Qi et al., 2011a)....

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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