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Journal ArticleDOI

Intracortical and Thalamocortical Connections of the Hand and Face Representations in Somatosensory Area 3b of Macaque Monkeys and Effects of Chronic Spinal Cord Injuries.

30 Sep 2015-The Journal of Neuroscience (Society for Neuroscience)-Vol. 35, Iss: 39, pp 13475-13486
TL;DR: It is shown that reorganization of primary somatosensory area 3b is not accompanied with either an increase in intrinsic cortical connections between the hand and face representations, or any change in thalamocortical inputs to these areas.
Abstract: Brains of adult monkeys with chronic lesions of dorsal columns of spinal cord at cervical levels undergo large-scale reorganization. Reorganization results in expansion of intact chin inputs, which reactivate neurons in the deafferented hand representation in the primary somatosensory cortex (area 3b), ventroposterior nucleus of the thalamus and cuneate nucleus of the brainstem. A likely contributing mechanism for this large-scale plasticity is sprouting of axons across the hand-face border. Here we determined whether such sprouting takes place in area 3b. We first determined the extent of intrinsic corticocortical connectivity between the hand and the face representations in normal area 3b. Small amounts of neuroanatomical tracers were injected in these representations close to the electrophysiologically determined hand-face border. Locations of the labeled neurons were mapped with respect to the detailed electrophysiological somatotopic maps and histologically determined hand-face border revealed in sections of the flattened cortex stained for myelin. Results show that intracortical projections across the hand-face border are few. In monkeys with chronic unilateral lesions of the dorsal columns and expanded chin representation, connections across the hand-face border were not different compared with normal monkeys. Thalamocortical connections from the hand and face representations in the ventroposterior nucleus to area 3b also remained unaltered after injury. The results show that sprouting of intrinsic connections in area 3b or the thalamocortical inputs does not contribute to large-scale cortical plasticity. Significance statement: Long-term injuries to dorsal spinal cord in adult primates result in large-scale somatotopic reorganization due to which chin inputs expand into the deafferented hand region. Reorganization takes place in multiple cortical areas, and thalamic and medullary nuclei. To what extent this brain reorganization due to dorsal column injuries is related to axonal sprouting is not known. Here we show that reorganization of primary somatosensory area 3b is not accompanied with either an increase in intrinsic cortical connections between the hand and face representations, or any change in thalamocortical inputs to these areas. Axonal sprouting that causes reorganization likely takes place at subthalamic levels.
Citations
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Journal ArticleDOI
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.

109 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...In fact, there is little anatomical evidence that the face-elicited activity in SI is mediated by the growth of new cortico-cortical projections: Very few axons cross the face–hand boundary in SI of intact animals (see [57] for analogous results in humans revealed with neuroimaging) and deafferentation of the hand region does not result in any measurable increase in these boundary-crossing projections [58]....

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Journal ArticleDOI
23 Aug 2016-eLife
TL;DR: It is shown that representation of the missing hand’s individual fingers persists in the primary somatosensory cortex even decades after arm amputation, questions the extent to which continued sensory input is necessary to maintain organisation in sensory cortex, thereby reopening the question what happens to a cortical territory once its main input is lost.
Abstract: The hand area of the primary somatosensory cortex contains detailed finger topography, thought to be shaped and maintained by daily life experience. Here we utilise phantom sensations and ultra high-field neuroimaging to uncover preserved, though latent, representation of amputees' missing hand. We show that representation of the missing hand's individual fingers persists in the primary somatosensory cortex even decades after arm amputation. By demonstrating stable topography despite amputation, our finding questions the extent to which continued sensory input is necessary to maintain organisation in sensory cortex, thereby reopening the question what happens to a cortical territory once its main input is lost. The discovery of persistent digit topography of amputees' missing hand could be exploited for the development of intuitive and fine-grained control of neuroprosthetics, requiring neural signals of individual digits.

97 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...…more limited than initially thought, and that instead the functional changes previously observed in S1 following input loss could be attributed to reorganisation in sub-cortical areas in the afferent pathway, principally the brainstem (Jain et al., 1998; Kambi et al., 2014; Chand and Jain, 2015)....

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Journal ArticleDOI
TL;DR: The need to consider potential contributions of additional brain mechanisms, beyond S1 remapping, and the dynamic interplay of contextual factors with brain changes for understanding and alleviating PLP is highlighted.

70 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...It has been suggested that the initial remapping triggered by deprivation will become refined by inputs due to daily hand usage involving compensatory behaviours (Churchill et al., 1998; Elbert et al., 1997)....

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Journal ArticleDOI
TL;DR: The data extend the Brodmann model in human sensorimotor cortex and suggest that body parts are an important organizing principle, similar to the distinction between sensory and motor processing.
Abstract: The cytoarchitectonic map as proposed by Brodmann currently dominates models of human sensorimotor cortical structure, function, and plasticity. According to this model, primary motor cortex, area 4, and primary somatosensory cortex, area 3b, are homogenous areas, with the major division lying between the two. Accumulating empirical and theoretical evidence, however, has begun to question the validity of the Brodmann map for various cortical areas. Here, we combined in vivo cortical myelin mapping with functional connectivity analyses and topographic mapping techniques to reassess the validity of the Brodmann map in human primary sensorimotor cortex. We provide empirical evidence that area 4 and area 3b are not homogenous, but are subdivided into distinct cortical fields, each representing a major body part (the hand and the face). Myelin reductions at the hand-face borders are cortical layer-specific, and coincide with intrinsic functional connectivity borders as defined using large-scale resting state analyses. Our data extend the Brodmann model in human sensorimotor cortex and suggest that body parts are an important organizing principle, similar to the distinction between sensory and motor processing.

63 citations


Cites background from "Intracortical and Thalamocortical C..."

  • ...However, a recent definitive study showed that in monkeys with chronic lesions of the dorsal column of spinal cord that had resulted in large-scale map reorganization of hand and face representations in area 3b, nevertheless showed a striking absence of new intracortical projections across the hand–face border (Chand and Jain 2015)....

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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

References
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Journal ArticleDOI

259 citations


"Intracortical and Thalamocortical C..." refers background or result in this paper

  • ...These locations correspond to representations of D1 and chin in the VP nucleus (Jones and Friedman, 1982; Kaas et al., 1984; Darian-Smith et al., 1990; Burton and Fabri, 1995; Padberg et al., 2009)....

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  • ...Normal thalamocortical connections and the somatotopy in the VP nucleus of thalamus have been described by many laboratories, and our data conform to previous reports (Jones and Friedman, 1982; Darian-Smith et al., 1990; Krubitzer and Kaas, 1992; Padberg et al., 2009; Cerkevich et al., 2013)....

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Journal ArticleDOI
06 Nov 1998-Science
TL;DR: Reorganization of brainstem and thalamic nuclei associated with slow transneuronal atrophy is likely to be a progressive process and when coupled with divergence of ascending connections, it islikely to make a substantial contribution to representational changes in cortex.
Abstract: After long-term denervation of an upper limb in macaque monkeys, the representation of the face in somatosensory cortex expands over many millimeters into the silenced representation of the hand. Various brainstem and cortical mechanisms have been proposed to explain this phenomenon. Reorganization in the thalamus has been largely ignored. In monkeys with deafferented upper limbs for 12 to 20 years, it was found that the brainstem cuneate and the thalamic ventral posterior nuclei had undergone severe transneuronal atrophy, and physiological mapping in the thalamus revealed that the face and trunk representations were adjoined while the normally small representation of the lower face had expanded comparable to the expansion in cortex. Reorganization of brainstem and thalamic nuclei associated with slow transneuronal atrophy is likely to be a progressive process. When coupled with divergence of ascending connections, it is likely to make a substantial contribution to representational changes in cortex.

246 citations


"Intracortical and Thalamocortical C..." refers background in this paper

  • ...Axonal sprouting that causes reorganization likely takes place at subthalamic levels. the thalamus (Jones and Pons, 1998; Kaas et al., 1999; Jain et al., 2008), and cuneate nucleus of the brainstem (Kambi et al., 2014)....

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  • ...Role of intrinsic connections in plasticity Intrinsic connections likely contribute to the brain reorganization (Burton and Fabri, 1995; Jones and Pons, 1998)....

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  • ...…afferents from VPM into the deafferented hand area, or VPL into the face region of area 3b. Previously, extensive shrinkage of VP nucleus has been reported in monkeys with dorsal root sections, which was proposed to be a likely mediator of large-scale brain plasticity (Jones and Pons, 1998)....

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Journal ArticleDOI
TL;DR: The results reveal that while connectivity between similar compartments predominates (e.g., blob to blob, right eye column toright eye column), interactions do occur between functionally different regions.
Abstract: To help understand the role of long-range, clustered lateral connections in the superficial layers of macaque striate cortex (area V1), we have examined the relationship of the patterns of intrinsic connections to cytochrome oxidase (CO) blobs, interblobs, and ocular dominance (OD) bands, using biocytin based neuroanatomical tracing, CO histochemistry, and optical imaging. Microinjections of biocytin in layer 3 resulted in an asymmetric field (average anisotropy of 1.8; maximum spread--3.7 mm) of labeled axon terminal clusters in layers 1-3, with the longer axis of the label spread oriented orthogonal to the rows of blobs and imaged OD stripes, parallel to the V1/V2 border. These labeled terminal patches (n = 186) from either blob or interblob injections (n = 20) revealed a 71% (132 out of 186) commitment of patches to the same compartment as the injection site; 11% (20 out of 186) to the opposite compartment, and 18% (34 out of 186) to borders of blob-interblob compartments, indicating that the connectivity pattern is not strictly blob to blob, or interblob to interblob (p < 0.005; chi(2)). In injections placed within single OD domains (n = 11), 54% of the resulting labeled terminal patches (43 out of 79) fell into the same OD territories as the injection sites, 28% (22 out of 79) into the opposite OD regions, and 18% (14 out of 79) on borders, showing some connectional bias toward same-eye compartments (p < 0.02; ANOVA). Individual injection cases, however, varied in the degree (50-100% for CO patterns, 22-100% for OD patterns) to which they showed same-compartment connectivity. These results reveal that while connectivity between similar compartments predominates (e.g., blob to blob, right eye column to right eye column), interactions do occur between functionally different regions.

205 citations


"Intracortical and Thalamocortical C..." refers background in this paper

  • ...Intrinsic connections restricted to functional compartments have been observed in other systems, including visual, auditory, and motor cortex (Huntley and Jones, 1991; Yoshioka et al., 1996; Read et al., 2001; Ahmed et al., 2012)....

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Journal ArticleDOI
03 Apr 1997-Nature
TL;DR: Sensory stimuli to the body are conveyed by the spinal cord to the primary somatosensory cortex, which is highly dependent on dorsal spinal column inputs, and other spinal pathways do not substitute for the dorsal columns even after injury.
Abstract: Sensory stimuli to the body are conveyed by the spinal cord to the primary somatosensory cortex. It has long been thought that dorsal column afferents of the spinal cord represent the main pathway for these signals, but the physiological and behavioural consequences of cutting the dorsal column have been reported to range from mild and transitory to marked. We have re-examined this issue by sectioning the dorsal columns in the cervical region and recording the responses to hand stimulation in the contralateral primary somatosensory cortex (area 3b). Following a complete section of the dorsal columns, neurons in area 3b become immediately and perhaps permanently unresponsive to hand stimulation. Following a partial section, the remaining dorsal column afferents continue to activate neurons within their normal cortical target territories, but after five or more weeks the area of activation is greatly expanded. After prolonged recovery periods of six months or more, the deprived hand territory becomes responsive to inputs from the face (which are unaffected by spinal cord section). Thus, area 3b of somatosensory cortex is highly dependent on dorsal spinal column inputs, and other spinal pathways do not substitute for the dorsal columns even after injury.

195 citations


"Intracortical and Thalamocortical C..." refers background in this paper

  • ...…of intact chin inputs into the deafferented hand region of primary somatosensory area 3b, second somatosensory area S2, parietal ventral area PV (Jain et al., 1997, 1998a; Kaas et al., 2008; Tandon et al., 2009), ventroposterior (VP) nucleus of Received May 26, 2015; revised Aug. 24, 2015;…...

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  • ...We extend these observations and show that chin representation also has only few connections across the hand– face border, which is important because it is the chin representation that expands as a result of massive deafferentations (Pons et al., 1991; Jain et al., 1997, 2008)....

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Journal ArticleDOI
TL;DR: Coincident labeling of thalamocortical neuron populations with different dyes increased the precision with which their soma distributions could be related within thalamic space, and enabled the detection by double labeling, of individualThalamic neurons that were common to the thalamate distributions projecting to separate, dye‐injected cortical zones.
Abstract: We used several fluorescent dyes (Fast Blue, Diamidino Yellow, Rhodamine Latex Microspheres, Evans Blue, and Fluoro-Gold) in each of eight macaques, to examine the patterns of thalamic input to the sensorimotor cortex of macaques 12 months or older. Inputs to different zones of motor, premotor, and postarcuate cortex, supplementary motor area, and areas 3b/1 and 2/5 in the postcentral cortex, were examined. Coincident labeling of thalamocortical neuron populations with different dyes (1) increased the precision with which their soma distributions could be related within thalamic space, and (2) enabled the detection by double labeling, of individual thalamic neurons that were common to the thalamic soma distributions projecting to separate, dye-injected cortical zones. Double-labeled thalamic neurons projecting to sensorimotor cortex were rarely seen in mature macaques, even when the injection sites were only 1–1.5 mm apart, implying that their terminal arborizations were quite restricted horizontally. By contrast, separate neuron populations in each thalamic nucleus with input to sensorimotor cortex projected to more than one cytoarchitecturally distinct cortical area. In ventral posterior lateral (oral) (VPLo), for example, separate populations of cells sent axons to precentral medial, and lateral area 4, medial premotor, and postarcuate cortex, as well as to supplementary motor area. Extensive convergence of thalamic input even to the smallest zones of dye uptake in the cortex (≈0.5 mm3) characterized the sensorimotor cortex. The complex forms of these projection territories were explored using 3-dimensional reconstructions from coronal maps. These projection territories, while highly ordered, were not contained by the cytoarchitectonic boundaries of individual thalamic nuclei. Their organization suggests that the integration of the diverse information from spinal cord, cerebellum, and basal ganglia that is needed in the execution of complex sensorimotor tasks begins in the thalamus.

193 citations


"Intracortical and Thalamocortical C..." refers background or result in this paper

  • ...These locations correspond to representations of D1 and chin in the VP nucleus (Jones and Friedman, 1982; Kaas et al., 1984; Darian-Smith et al., 1990; Burton and Fabri, 1995; Padberg et al., 2009)....

    [...]

  • ...Normal thalamocortical connections and the somatotopy in the VP nucleus of thalamus have been described by many laboratories, and our data conform to previous reports (Jones and Friedman, 1982; Darian-Smith et al., 1990; Krubitzer and Kaas, 1992; Padberg et al., 2009; Cerkevich et al., 2013)....

    [...]