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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
Tina Kao1, Jed S. Shumsky1, Eric B. Knudsen1, Marion Murray1, Karen A. Moxon1 
TL;DR: Cortical neurons recorded from neonatally spinalized rats that received exercise had higher spontaneous firing rates, were more likely to respond to both sensory and sensorimotor stimulations of the forelimbs, and responded with more spikes per stimulus than those recorded from normal rats, suggesting expansion of the Forelimb map into the hind Limb map.
Abstract: Spinal cord transection silences neuronal activity in the deafferented cortex to cutaneous stimulation of the body and untreated animals show no improvement in functional outcome (weight-supported ...

31 citations


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

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

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Journal ArticleDOI
TL;DR: This review focuses on the reorganization of cortical networks observed after injury and posits a role of intracortical circuits in recovery.

31 citations

Journal ArticleDOI
TL;DR: It is suggested that the ways in which structures and brain mechanisms react to missing or critically altered sensory and motor peripheral signals are variably affected across multiple timescales and may contribute to the appearance of secondary pathological conditions, such as allodynia, hyperalgesia, and neuropathic pain.
Abstract: Neuroplastic changes in somatotopic organization within the motor and somatosensory systems have long been observed. The interruption of afferent and efferent brain-body pathways promotes extensive cortical reorganization. Changes are majorly related to the typical homuncular organization of sensorimotor areas and specific "somatotopic interferences". Recent findings revealed a relevant peripheral contribution to the plasticity of body representation in addition to the role of sensorimotor cortices. Here, we review the ways in which structures and brain mechanisms react to missing or critically altered sensory and motor peripheral signals. We suggest that these plastic events are: (i) variably affected across multiple timescales, (ii) age-dependent, (iii) strongly related to altered perceptual sensations during and after remapping of the deafferented peripheral area, and (iv) may contribute to the appearance of secondary pathological conditions, such as allodynia, hyperalgesia, and neuropathic pain. Understanding the considerable complexity of plastic reorganization processes will be a fundamental step in the formulation of theoretical and clinical models useful for maximizing rehabilitation programs and resulting recovery.

30 citations


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

  • ...These changes include the expansion of new facial connections into the deafferented hand region (in the primary somatosensory cortex [15] and the ventroposterior nucleus of the thalamus [16], spinal cord, and dorsal column nuclei [17]) as well as the transneuronal atrophy of deafferented structures [18]....

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Journal ArticleDOI
TL;DR: The tongue representation appeared to be unique in area 3b in that it also received inputs from areas in the anterior upper bank of the lateral sulcus and anterior insula that may include the primary gustatory area (area G) and other cortical taste‐processing areas, as well as a region of lateral prefrontal cortex (LPFC) lining the principal sulcus.
Abstract: We placed injections of anatomical tracers into representations of the tongue, teeth, and face in the primary somatosensory cortex (area 3b) of macaque monkeys. Our injections revealed strong projections to representations of the tongue and teeth from other parts of the oral cavity responsive region in 3b. The 3b face also provided input to the representations of the intraoral structures. The primary representation of the face showed a pattern of intrinsic connections similar to that of the mouth. The area 3b hand representation provided little to no input to either the mouth or the face representations. The mouth and face representations of area 3b received projections from the presumptive oral cavity and face regions of other somatosensory areas in the anterior parietal cortex and the lateral sulcus, including areas 3a, 1, 2, the second somatosensory area (S2), the parietal ventral area (PV), and cortex that may include the parietal rostral (PR) and ventral somatosensory (VS) areas. Additional inputs came from primary motor (M1) and ventral premotor (PMv) areas. This areal pattern of projections is similar to the well-studied pattern revealed by tracer injections in regions of 3b representing the hand. The tongue representation appeared to be unique in area 3b in that it also received inputs from areas in the anterior upper bank of the lateral sulcus and anterior insula that may include the primary gustatory area (area G) and other cortical taste-processing areas, as well as a region of lateral prefrontal cortex (LPFC) lining the principal sulcus.

30 citations


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

  • ...The somatotopic organization in area 3b is indicated: OC, oral cavity; Fa, face; H, hand; A, arm; O, occiput; T, trunk; L, leg; Ft, foot (adapted from Nelson et al., 1980; Jain et al., 2008)....

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  • ...…its large size, functional importance in evaluating and processing food (Shepherd, 2012), expansion after spinal cord injury (Pons et al., 1991; Jain et al., 1997, 1998b, 2008; Fang et al., 2002), and role in coordinating movements of the tongue and jaw (Lin et al., 1993, 1994), little is…...

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  • ...…Kaas, 1995) and deafferenting injuries of the peripheral nerves (Merzenich et al., 1983a,b; Garraghty and Kaas, 1991; Garraghty et al., 1994) and spinal cord (Pons et al., 1991; Jain et al., 1997, 1998b, 2008) can lead to changes in the responsiveness of the region of area 3b representing the hand....

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  • ...Reorganization in the somatosensory cortex after such injuries often results in hand cortex becoming responsive to stimulation on the face (Merzenich et al., 1984; Pons et al., 1991; Florence and Kaas, 1995; Jain et al., 1997, 1998b, 2008; Manger et al., 1997)....

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  • ...…allowed us to evaluate the possibility that intrinsic connections between hand and face representations in area 3b underlie the reactivation of hand cortex by inputs from the face after loss of sensory input from the hand (Pons et al., 1991; Jain et al., 1997, 1998b, 2008; Fang et al., 2002)....

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Book ChapterDOI
01 Jan 2012

29 citations

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